Introduction
The harvesting of wild meat for human consumption is among the greatest threats to tropical wildlife and is a primary cause of population declines (Bennett et al., Reference Bennett, Blencowe, Brandon, Brown, Burn and Cowlishaw2007). Aside from conservation concerns, unsustainable harvesting of wild meat can also jeopardize livelihoods and food security (Nasi et al., Reference Nasi, Taber and van Vliet2011). Characterizing the dynamics of wild-meat harvesting and consumption is challenging because of interactions among bio-physical variables (e.g. urban remoteness, species ecology) and social factors (e.g. poverty, cultural preferences; Brashares et al., Reference Brashares, Golden, Weinbaum, Barrett and Okello2011; Dupain et al., Reference Dupain, Nackoney, Mario Vargas, Johnson, Farfán, Bofaso and Fa2012). Despite its inherent complexity, harvesting of wild meat is frequently dichotomized as a subsistence activity for the marginalized rural poor (de Merode et al., Reference de Merode, Homewood and Cowlishaw2004) or a lucrative commercial endeavour supplying urban markets with a luxury heritage item (East et al., Reference East, Kümpel, Milner-Gulland and Rowcliffe2005). Legislation often reinforces this polarization by allowing the former but not the latter. The commercialization of wild meat for urban markets is considered to be the primary driver of the bushmeat crisis in West and Central Africa (Bennett et al., Reference Bennett, Blencowe, Brandon, Brown, Burn and Cowlishaw2007).
In the Neotropics, examination of wild-meat harvesting and consumption has centred on the rural subsistence paradigm (Peres, Reference Peres2000). In Amazonia research has focused mainly on the determinants and ecological impacts of rural hunting practices (Peres & Nascimento, Reference Peres and Nascimento2006). Regional estimates of bushmeat consumption have been extrapolated from rural village-level offtake studies (Peres, Reference Peres2000; Fa et al., Reference Fa, Peres and Meeuwig2002) but these estimates ignore commercial trade and urban consumption, instead assuming that urban Amazonians do not eat forest wildlife (Nasi et al., Reference Nasi, Taber and van Vliet2011). This assumption must now be re-examined, given evidence of high levels of commercialization and consumption of wild meat in Amazonian cities (Parry et al., Reference Parry, Barlow and Pereira2014; van Vliet et al., Reference van Vliet, Quiceno-Mesa, Cruz-Antia, Aquino, Moreno and Nasi2014). With rapid growth of cities, aggregate urban consumption of wild meat in Amazonia could be vast and increasing, yet the interacting dynamics of rural harvest, trade networks and urban markets remain under-studied.
Urban consumption of wildlife often requires long-distance trade networks connecting distal forests with metropolitan consumers. In Asia, for example, turtle meat is traded across international borders (Nijman, Reference Nijman2010) and significant quantities of African bushmeat end up in illegal meat markets in Europe (Chaber et al., Reference Chaber, Allebone-Webb, Lignereux, Cunningham and Rowcliffe2010). Even within national boundaries networks can span vast distances, and harvesters will travel further to meet demand as wildlife populations decline (Lindsey et al., Reference Lindsey, Balme, Becker, Begg, Bento and Bocchino2013). Examining wildlife harvest and trade over large spatial scales is problematic for researchers because of the time and cost of fieldwork, and the difficulty of studying an often illegal and cryptic activity (Razafimanahaka et al., Reference Razafimanahaka, Jenkins, Andriafidison, Randrianandrianina, Rakotomboavonjy, Keane and Jones2012). In Amazonia, where so little is known about the scale and nature of urban consumption of wild meat, an important step is to synthesize present understanding and define key knowledge gaps to inform applied research and policy interventions. We use an expert elicitation approach to gauge knowledge, using caiman as a model taxon for understanding large-scale patterns of wildlife harvest, trade and consumption.
Caiman: a model taxon
There is a significant lack of knowledge about current levels of harvesting, trade and consumption of caiman in Amazonia. Harvest studies tend to focus on terrestrial mammals, as they are considered to be preferred by hunters and have long been studied by tropical ecologists (Bodmer, Reference Bodmer1995; Peres & Nascimento, Reference Peres and Nascimento2006). In contrast, caimans are considered to be a localized, secondary source of protein (Thorbjarnarson, Reference Thorbjarnarson2010), and as such their extent and role in Amazonian diets is comparatively unknown. Two caiman species in particular are harvested and consumed in Amazonia: the black caiman Melanosuchus niger and the spectacled caiman Caiman crocodilus. They are the two largest crocodilian species in the region and both have a long history of human exploitation, having been commercially hunted for their skins to supply international demand for exotic leather throughout much of the 20th century. Sanctions on international trade facilitated the recovery of many populations, notably those of the black caiman, which were all but decimated by overharvesting, and both species are categorized as Least Concern on the IUCN Red List (Crocodile Specialist Group, 1996; Ross, Reference Ross2000).
Based on a few localized rural harvest studies, consumption of caiman has been recorded in various localities across Amazonia (Ojasti, Reference Ojasti1996); using extrapolated data Peres (Reference Peres2000) estimated annual harvest rates of caiman meat by the rural poor in the Brazilian Amazon to be 240–589 t (by 25,000–62,000 individuals). There is now some evidence that caiman meat is traded commercially and consumed in urban areas (Baía et al., Reference Baía, Guimarães and Le Pendu2010; Parry et al., Reference Parry, Barlow and Pereira2014); however, much of our knowledge remains anecdotal (Thorbjarnarson, Reference Thorbjarnarson2010). Additionally, caiman meat may be sold fraudulently as a high-value prestige fish (Peres & Carkeek, Reference Peres and Carkeek1993). Fraudulent meat substitution is a global concern (e.g. Europe's horsemeat scandal; Di Giuseppe et al., Reference Di Giuseppe, Giarretta, Lippert, Severino and Di Maro2015) and an important conservation issue (von der Heyden et al., Reference von der Heyden, Barendse, Seebregts and Matthee2010). The use of caiman (together with river dolphins Inia geoffrensis) as fish bait is also a concern following increased international demand for the catfish Calophysus macropterus (Mintzer et al., Reference Mintzer, Martin, da Silva, Barbour, Lorenzen and Frazer2013). Our aim here was to enhance understanding of what is a potentially multifaceted and spatially extensive harvesting and trade system.
Methods
We used an expert survey approach to obtain information on patterns and drivers of harvesting and trade of caiman across the Brazilian Amazon. The increasing use of expert elicitation in conservation research and planning has been driven by the need to characterize dynamic systems, with limited resources (Martin et al., Reference Martin, Burgman, Fidler, Kuhnert, Low-Choy, McBride and Mengersen2012). The method is an expedient approach for obtaining a regional synthesis of a politically invisible issue about which local experts may be aware (van Vliet et al., Reference van Vliet, Adams, Vieira and Mertz2013).
We approached 122 experts to participate in the survey, based on relevant professional experience and/or current employment. We targeted people working in situ on caiman harvesting or management in the Brazilian Amazon, as well as other locally based individuals with current expert knowledge and professional experience of conservation and natural resource management. We identified potential respondents as follows: (1) authors identified in relevant literature, (2) reserve managers (including of federal and state protected areas), and (3) researchers and analysts from academic institutions or federal government environmental institutions, such as the Brazilian Institute of Environment and Renewable Natural Resources (IBAMA, responsible for enforcing environmental law outside protected areas) and the Chico Mendes Institute of Biodiversity Conservation (ICMBio, with a mandate for enforcement within federal protected areas). Contact was made via e-mail during September−November 2013; e-mail addresses were obtained through known contacts, via author information provided with published articles, or from institutional websites. An initial e-mail explained the objectives of the research, sought consent to participate and included a questionnaire as an attachment. Respondents were asked to indicate other potential participants, thus expanding our contact database. In total we received 52 responses (whether accepting or declining the invitation to participate), with 24 completed questionnaires (20% of the 122 approached). This response rate is consistent with other expert surveys (23%, Lyytimäki & Hildén, Reference Lyytimäki and Hildén2011; 23%, Quijas et al., Reference Quijas, Jackson, Maass, Schmid, Raffaelli and Balvanera2012).
The questionnaire (Supplementary Material 1) consisted of 11 statements, which participants were asked to rate on a Likert scale (Likert, Reference Likert1932), from 1 (completely disagree) to 5 (completely agree). Statements were related to relevant topics and knowledge gaps identified in a literature review, including the following: occurrence and drivers of caiman harvesting and trade, characteristics of harvesters, fraudulent meat substitution, and use of caiman meat as fish bait. We included a 2-year qualifier for questions that related to temporal trends (such as harvesting levels and caiman populations). This relatively short qualifier was chosen to focus on current harvesting (as opposed to historical trends) and also accounts for the rotation (change of location) of staff in government agency positions. Respondents also provided information on their employment role and the area or municipality from which their experience was derived. At the end of the questionnaire respondents were invited to explain the rationale for their responses and offer any other relevant information on hunting and trade of caiman in their region.
The 24 responses covered a wide area of the Brazilian Amazon, from the eastern city of Belém to the western border town of Tabatinga. The majority of responses were from experts based in Amazonas State (17 questionnaires, 71%). Of the remaining seven questionnaires five were from experts based in Pará State (21%). We also received one response each from the states of Mato Grosso and Mato Grosso do Sul; however, as these responses were from outside the Amazon biome we focus on Amazonas and Pará, which together cover 56% of the Brazilian Legal Amazon and are home to 48% of the region's human population (IBGE, 2010).
Results
The majority of experts (76%; Fig. 1) agreed (partially or completely) that caiman hunting was a common occurrence, extending across the Brazilian Amazon, from Santarém to Tabatinga on the Brazil−Colombia border (Fig. 2). Whether caiman hunting was premeditated rather than opportunistic (e.g. by fishers) generated a more mixed response (Fig. 1), even between proximate localities. Temporal trends in harvesting pressure were also unclear, with 68% of experts unable to affirm or refute that the occurrence of caiman hunting had increased in the previous 2 years. There was no apparent indication of a contemporary, widespread decline of caiman populations. Only one respondent considered local caiman populations to be decreasing, whereas 43% disagreed with this assertion and 52% were uncertain (Fig. 1).
Fig. 1 Expert responses on the scale and drivers of caiman harvesting and trade in the Brazilian Amazon. Respondents rated each statement on a five-point scale, based on their perceptions and experience within their locale.
Fig. 2 Spatial distribution of expert responses, on a Likert scale, to the following statements regarding the harvesting and trade of caiman in the Brazilian states of Amazonas (AM) and Pará (PA): (a) Caiman hunting is a common occurrence. (b) Caiman hunters live in rural areas. (c) Caiman meat is a source of protein in rural areas. (d) Caiman are hunted to supply urban markets. (e) Caiman meat is sold fraudulently as high-value fish. (f) Caiman are hunted for bait to capture piracatinga Calophysus macropterus.
Our results indicated that demand for caiman meat came from both urban and rural consumers. Urban demand for caiman meat was recognized by 64% of the experts (Fig. 1), and harvesting caiman to supply urban markets was reportedly concentrated along the River Solimões−Amazonas and proximate sections of its tributaries (Fig. 2). Suggestive of distal source areas, a respondent in Belém stated that caiman meat was sold in urban markets and consumed in local rural areas but was not harvested locally (Fig. 2). A respondent based in Amazonas [R1] elaborated on this potential long-distance trade:
Ribeirinho [river-dwellers] hunters kill caiman indiscriminate of species or sex…100% of the meat is salted and dried, to be sold to traders from the state of Pará. From there it is sold in urban markets around the capital of Belém.
Another respondent based in Amazonas [R18] attributed this to different regional food preferences:
I always hear talk that people who like caiman meat are from Pará, and that people from Amazonas do not like caiman meat.
Whether hunters supplying the urban market were from rural or urban areas was unclear. More than half the experts disagreed that urban-based hunters were operating. However, 24% of respondents were uncertain and 16% completely agreed that urban hunters contribute significantly to the caiman meat market. Overall, there was stronger evidence that caiman were predominantly hunted by rural people (64%), and that harvesting was to supply rural people with animal protein (52%). The clearest evidence (i.e. strong agreement) of rural consumption came from around the major urban centres (Fig. 2). In summary, expert opinion indicates that caiman are hunted mainly by rural people, providing a source of protein to rural communities close to larger cities, and a source of income when sold to urban markets, particularly along the main River Solimões−Amazonas.
There was uncertainty regarding whether caiman were hunted for fish bait or whether caiman meat was sold fraudulently as fish (Fig. 1). The strongest evidence of fishers using caiman meat as bait was from along the River Solimões−Amazonas, from Santarém through to Tabatinga. There was disagreement or uncertainty in most other locations (Fig. 2). It was unclear whether this practice was increasing, as half of the respondents were uncertain of any temporal trend. Fraudulent selling of caiman meat as high-value fish appeared to be less widespread than using caiman as fish bait, with approximately equal numbers of experts expressing uncertainty (32%), agreeing that this happens in their area (36%), and disagreeing (32%). Strong agreement that such fraud occurs came from around the major cities of Manaus, Santarém and Belém (Fig. 2).
Discussion
Our findings demonstrate that expert elicitation is an effective method for evaluating wildlife harvest over large spatial scales. The respondents offered novel insights into a complex harvest system in the Brazilian Amazon, including widespread harvesting, urban demand and long-distance trade, and the extent of lesser-known secondary drivers. We acknowledge the limitations of the use of expert surveys for generating knowledge from individual judgement, given potential bias and varying levels of expertise (Kynn, Reference Kynn2008). Nonetheless we believe expert elicitation is an appropriate, cost-effective approach to perform a rapid regional synthesis of a poorly known and complex issue. Viewed pragmatically, the information we obtained here is a valuable precursor to empirical data collection and we highlight the need for validating the expert knowledge underlying our findings (Kynn, Reference Kynn2008; Keane, Reference Keane2013).
Key insights and interpretations
It was assumed that Amazonia had avoided a bushmeat crisis on the basis of urbanization and assertions that the only wild meat eaten by city-dwellers was fish (Nasi et al., Reference Nasi, Taber and van Vliet2011). However, expert opinion indicates that killing caiman for meat, previously considered a localized rural activity (Peres, Reference Peres2000), is in fact common and widespread across the Brazilian Amazon. We also found that urban demand is a significant driver of the harvest, with trade of caiman meat concentrated around large urban centres. Spatial patterns of expert responses and direct quotes support previous anecdotal evidence of long-distance trade in caiman meat from the state of Amazonas to Pará (Da Silveira & Thorbjarnarson, Reference Da Silveira and Thorbjarnarson1999). Long-distance trade suggests substantial demand that offsets higher costs for processing and transport, together with the presence of commodity chains and trade networks (Lindsey et al., Reference Lindsey, Balme, Becker, Begg, Bento and Bocchino2013). It also implies that demand for caiman meat cannot be fulfilled by local sources and could therefore be a symptom of local overharvesting and depletion (Lindsey et al., Reference Lindsey, Balme, Becker, Begg, Bento and Bocchino2013).
Market price data from a study in Pará showed that caiman meat is cheaper than fresh or dried beef, with prices comparable to chicken, shrimp and fish (Baía et al., Reference Baía, Guimarães and Le Pendu2010). This implies that caiman meat in the Amazon does not fit the luxury good paradigm often documented in urban wild-meat consumption (Bennett, Reference Bennett2002). Instead, we infer that caiman meat provides a cheap alternative protein option for the urban poor, congruent with evidence of poverty-linked caiman consumption in two provincial cities (Parry et al., Reference Parry, Barlow and Pereira2014). Regardless of access to domestic protein sources, poverty will drive demand for cheaper alternatives. With > 70% of the rapidly growing population in the Brazilian Amazon living in cities, including millions living in urban poverty (IBGE, 2010), we predict demand for caiman meat will remain high (or increase). Furthermore, rural–urban migrants often remain dependent on rural livelihoods (Parry et al., Reference Parry, Barlow and Pereira2014) and many Amazonian households can be described as multi-sited, participating in rural–urban networks (Padoch et al., Reference Padoch, Brondizio, Costa, Pinedo-Vasquez, Sears and Siqueira2008). Such patterns have important implications for wild-meat consumption, including the persistence of rural food preferences in Amazonian cities (Padoch et al., Reference Padoch, Brondizio, Costa, Pinedo-Vasquez, Sears and Siqueira2008). Parry et al. (Reference Parry, Barlow and Pereira2014) found that urban households with strong rural linkages are more likely to eat not just caiman but a range of wildlife.
Knowledge gaps and research priorities
Areas of uncertainty in expert opinion highlighted important knowledge gaps, which are crucial to identifying research priorities. Quantifying the role of urban demand on caiman harvesting and trade is a key knowledge gap. Data on trade routes, market structure and the drivers of hunter and consumer behaviour are needed, following a commodity-chain approach (Cowlishaw et al., Reference Cowlishaw, Mendelson and Rowcliffe2005; Allebone-Webb et al., Reference Allebone-Webb, Kümpel, Rist, Cowlishaw, Rowcliffe and Milner-Gulland2011). The African bushmeat crisis, defined as a critical conservation and development issue, has been studied extensively (Milner-Gulland & Bennett, Reference Milner-Gulland and Bennett2003; Allebone-Webb et al., Reference Allebone-Webb, Kümpel, Rist, Cowlishaw, Rowcliffe and Milner-Gulland2011; Lindsey et al., Reference Lindsey, Balme, Becker, Begg, Bento and Bocchino2013), and consequently we should reflect on this body of research to identify appropriate strategies and anticipate challenges. What is clear is the inherent variability and complexity of wild-meat trade and consumption patterns (Brashares et al., Reference Brashares, Golden, Weinbaum, Barrett and Okello2011), which limits broad generalizations and often requires case-specific information from both social development and ecological perspectives.
The fraudulent substitution of dried caiman meat for the sought-after fish Arapaima gigas is perhaps the biggest unknown factor in this study. We found that this fraud occurs around the large urban centres where food demand is highest, and recommend that this practice be quantitatively assessed to draw conclusions on its extent and impact. As this is a global issue in food production systems, there has been significant advancement in food authentication techniques (Mafra et al., Reference Mafra, Ferreira and Oliveira2008). DNA barcoding offers a relatively quick and inexpensive means of species identification and has been successfully used in bushmeat trade studies to confirm species misidentification (Minhós et al., Reference Minhós, Wallace, Ferreira da Silva, Sá, Carmo, Barata and Bruford2013); it is a viable option for assessing caiman–fish substitution.
The use of caiman (and river dolphins) as catfish bait has already been recognized as a significant concern, and the implementation of a 5-year moratorium on Calophysus macropterus fishing in Brazil is intended to curtail this practice (MMA, 2014). However, environmental governance in Amazonia is often poor because of limited resources and low enforcement over such a large area (Parry et al., Reference Parry, Barlow and Pereira2014). Continued assessment and monitoring is recommended.
Conclusion
The multidisciplinary nature of conservation means researchers must often utilize a diverse array of data sources and methods (Keane, Reference Keane2013). There is increasing recognition of the role of alternative approaches in wildlife conservation and management; for example, the use of recall data for species consumption rates (Golden et al., Reference Golden, Wrangham and Brashares2013) and of local ecological knowledge for wildlife abundance and distribution trends (Anadón et al., Reference Anadón, Giménez, Ballestar and Pérez2009). Such methods are particularly apposite in resource-limited and spatially extensive tropical contexts (Parry et al., Reference Parry, Barlow and Pereira2014). We used a simple expert elicitation method to gain insight into a complex and multifaceted harvesting system, and in doing so identified critical focal areas for further study, both thematically and spatially. Nonetheless we reiterate the importance of rigorous implementation of methods with regards to questionnaire design and interpretation of results (Martin et al., Reference Martin, Burgman, Fidler, Kuhnert, Low-Choy, McBride and Mengersen2012). Expert opinion is not a like-for-like substitute for empirical research but is a complementary, cost-effective tool that can inform and direct more intensive data collection, especially when confronting complex dynamic systems across large spatial scales.
Acknowledgements
The authors thank all the expert respondents who completed the questionnaire or offered comments and feedback. Financial support for this research was provided by Lancaster University, UK.
Biographical sketches
Natalie Swan previously worked on conservation and ecology of caiman in the Peruvian Amazon; her research interests now focus on large-scale patterns of wildlife consumption in Amazonia. Jos Barlow's research focuses on assessing and improving the value of human-modified tropical forests for biodiversity. Luke Parry is interested in identifying pathways towards sustainable urbanization in tropical forest regions, particularly the Amazon.
