Received: 4 February 2021 Revised: 24 May 2021 Accepted: 22 June 2021 DOI: 10.1111/cobi.13801 CONTRIBUTED PAPER Wild meat trade over the last 45 years in the Peruvian Amazon Pedro Mayor1,2,3,4 Hani R. El Bizri3,5,6,7 Thais Q. Morcatty5,6,7 Kelly Moya8 Nora Bendayán8 Samantha Solis8 Carlos F. A. Vasconcelos Neto6,7 Maire Kirkland9 Omar Arevalo10 Tula G. Fang2,3 Pedro E. Pérez-Peña11 Richard E. Bodmer2,3,12 1 Departament de Sanitat i d’Anatomia Animals, Abstract Facultat de Veterinària, Universitat Autònoma de The trade in wild meat is an important economic component of rural people’s livelihoods, Barcelona (UAB), Barcelona, Spain 2 but it has been perceived to be among the main causes of the decline of wildlife species. Museo de Culturas Indígenas Amazónicas, Iquitos, Peru Recently, the COVID-19 pandemic has brought to light an additional concern of wildlife 3 markets as a major human-health challenge. We analyzed data from the largest longitudinal ComFauna, Comunidad de Manejo de Fauna Silvestre en la Amazonía y en Latinoamérica, Iquitos, monitoring (1973–2018) of the most important urban wild-meat markets in Iquitos, Peru, Peru to examine the trends in and impacts of these markets on people’s livelihoods. Over the 4 Postgraduate Program in Animal Health and last 45 years, wild meat sales increased at a rate of 6.4 t/year (SD 2.17), paralleling urban Production in Amazonia (PPGSPAA), Federal Rural population growth. Wild meat sales were highest in 2018 (442 t), contributing US$2.6 mil- University of the Amazon (UFRA), Belém, Brazil lion (0.76%) to the regional gross domestic product. Five species of ungulates and rodents 5 Oxford Wildlife Trade Research Group, Oxford accounted for 88.5% of the amount of biomass traded. Vulnerable and Endangered species Brookes University (OBU), Oxford, UK represented 7.0% and 0.4% of individuals sold, respectively. Despite growth in sales, the 6 Rede de Pesquisa para Estudos sobre Diversidade, contribution of wild meat to overall urban diet was constant: 1–2%/year of total meat con- Conservação e Uso da Fauna na Amazônia (REDEFAUNA), Manaus, Brazil sumed. This result was due to greater availability and higher consumption of cheaper meats 7 (e.g., in 2018, poultry was 45.8% cheaper and was the most consumed meat) coupled with Mamirauá Sustainable Development Institute (IDSM), Tefé, Brazil the lack of economic incentives to harvest wild meat species in rural areas. Most wild meat 8 Universidad Nacional de la Amazonia Peruana was sold salted or smoked, reducing the likelihood of foodborne diseases. Community- (UNAP), Iquitos, Peru based wildlife management plans and the continued trade bans on primates and threat- 9 Durham University, Durham, UK ened taxa may avoid biodiversity loss. Considering the recent COVID-19 pandemic, future 10 management plans should include potential viral hosts and regulation and enforcement of Gerencia Regional de Asuntos Indígenas, Gobierno Regional de Loreto, Iquitos, Peru hygiene practices in wild-meat markets. 11 Instituto de Investigaciones de la Amazonía Peruana (IIAP), Iquitos, Peru KEYWORDS 12 Amazonia, bushmeat, mammals, public health, sustainability, urban markets, wildlife trade Durrell Institute of Conservation and Ecology, School of Anthropology and Conservation, University of Kent, Canterbury, UK Comercio de Carne de Monte en los Últimos 45 Años en la Amazonia Peruana Correspondence Resumen: El comercio de carne de monte es un componente económico importante Pedro Mayor, Departament de Sanitat i d’Anatomia del sustento de habitantes de zonas rurales, pero se ha percibido como una de las prin- Animals, Facultat de Veterinària, Universitat Autònoma de Barcelona (UAB), Barcelona 08193, cipales causas de la declinación de especies de vida silvestre. Recientemente, la pandemia Spain. de COVID-19 ha traído a la luz una preocupación adicional de los mercados de vida sil- Email: mayorpedro@hotmail.com vestre como un reto importante para la salud humana. Analizamos datos del monitoreo longitudinal más extenso (1973-2018) de los mercados urbanos de carne de monte más Article impact statement: Community-based importantes en Iquitos, Perú, para examinar las tendencias y los impactos de estos merca- wildlife management, trade bans for threatened taxa dos sobre el sustento de los habitantes. Las ventas de carne de monte incrementaron en This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made. © 2021 The Authors. Conservation Biology published by Wiley Periodicals LLC on behalf of Society for Conservation Biology Conservation Biology. 2021;1–13. wileyonlinelibrary.com/journal/cobi 1 2 MAYOR ET AL. and enforced hygiene practices in wild meat markets are needed to protect biodiversity and public health. los últimos 45 años a una tasa de 6.4 t/año (DS 2.17), en paralelo con el crecimiento de la población. Las ventas de carne de monte fueron más altas en 2018 (442 t), aportando U.S. $2.6 millones (0.76%) al producto interno bruto de la región. Cinco especies de ungulados y roedores comprendieron el 88.5% de la biomasa comercializada. Especies vulnerables y en peligro representaron 7.0% y 0.4% de los individuos vendidos, respectivamente. A pesar del incremento de las ventas, la contribución de la carne de monte al total de la dieta urbana fue constante: 1–2%/año del total de carne consumida. Este resultado se debió a una mayor disponibilidad y consumo de carnes más baratas (e. g., en 2018 la carne de pollo fue 45.8% más barata y fue la más consumida) aparejado con la falta de incentivos económicos para cosechar carne de especies silvestres en áreas rurales. La mayor parte de la carne de monte se vendía salada o ahumada, reduciendo con ello la probabilidad de enfermedades trans- mitidas por alimentos. Los planes de manejo de vida silvestre basados en comunidades y la prohibición continua del comercio de primates y taxa amenazados pueden evitar la pérdida de biodiversidad. Considerando la reciente pandemia de COVID-19, los planes de manejo futuros deben incluir potenciales huéspedes virales y la regulación y aplicación de prácticas de higiene en los mercados de carne de especies silvestres. PALABRAS CLAVE: Amazonía, carne de monte, comercio de vida silvestre, mamíferos, mercados urbanos, salud pública, sustentabil- idad : ,     ,   (1973–2018 ),     45 ,   6.4  (  2.17) ,  2018  (442 ),  260  (0.76%)    88.5%    7.0%0.4% ,  ,   1%–2% ( , 2018  45.8%, ),  ,   ,           ,    : ; :  :  , , , , , ,  INTRODUCTION health through the spillover of pathogens from wildlife (Roe & Lee, 2021). However, such calls are controversial because In tropical forests worldwide, wild meat represents a significant shutting markets down can ultimately backfire and cause severe source of animal protein and income for rural and urban people poverty and lack of food for many (Fa et al., 2015). Thus, (El Bizri et al., 2020; Fa et al., 2015). Recent overhunting of wild should the trade of wild meat be banned completely, or should meat species has been attributed, in part, to the integration of it be kept operating to some extent to continue to lessen rural rural and Indigenous populations into the market economy dur- poverty and ensure food and economic security? To make a ing the late 20th century. The improvement of river navigation fair and informed decision, detailed information on the wild and roads, plus the advent of new hunting technologies, led to meat trade can provide insights regarding their sustainability and an increase in supply and demand for wildlife products in urban guide the development of health protocols to avoid health risks centers (Chaves et al., 2017; Fa et al., 2015). Wild meat, there- to hunters, vendors, and consumers. fore, represents an increasingly important product for the econ- To date, much attention has focused on the sustainability and omy and survival of rural people (de Merode et al., 2004), and drivers of wild meat markets in West and Central Africa (de changes in sales of wild meat markets affect their livelihoods. Merode et al., 2004; Fa et al., 2015). However, wildlife markets Recently, the supposed connection between the SARS-CoV-2 are also important in the Amazon, yet few studies have been virus and wet markets in China resulted in several calls for bans conducted to assess the factors underlying wild meat trade in on wild meat because these markets may pose risks to human this region (van Vliet et al., 2014; El Bizri et al., 2020). One CONSERVATION BIOLOGY 3 exception is the long-term monitoring of wild meat trade in the and 2002 came from Castro et al. (1976), Bendayan (1991), urban markets of Iquitos, the largest city in the Peruvian Ama- Bodmer and Pezo (2001), and Bendayan and Bardales (2004), zon, which has involved intermittent data collection since 1973 respectively. More recently, we conducted market surveys in (Castro et al., 1976; Bendayan, 1991; Bodmer & Pezo, 2001; September 2006–August 2007, November 2013–October 2014, Mayor et al., 2019). and September 2017–August 2018. The Peruvian Ministry of Agriculture, through laws enacted We used long-term data gathered using similar survey meth- in 1976 (number 21147), 2000 (number 27308), and 2011 (num- ods from the same markets in Iquitos to assess changes in wild ber 29763), only authorized the sale of wild meat from areas meat sales through time. In all surveys, interviews with mar- with planned sustainable wildlife management. However, these ket vendors were conducted and meat counts were taken daily wildlife management practices are administratively difficult to or every 2 days. Castro et al. (1976) surveyed the markets of implement, and authorities have been unable to adequately Belén, Central, and Camal for 5 months. Surveys in 1986 and enforce these laws; thus, illegal sale of wild meat remains the 1987 (Bendayan, 1991), 1996 (Bodmer & Pezo, 2001), 2001 and norm. 2002 (Bendayan & Bardales, 2004), 2006 and 2007, and 2017 We assessed temporal trends from 1973 to 2018 in the and 2018 were conducted by our research group in the mar- amounts and prices of wild meat over the last 45 years in the kets of Belén and Modelo for 12 months. An additional survey main urban markets of Iquitos. We assessed the influence of was conducted by our team in 2013 and 2014 in the market of economic and sociocultural drivers, including human popula- Belén, and considering the representativeness of each market in tion, gross domestic product (GDP), and the domestic meat wild meat sales from the other surveys, a correction of 0.33 was supply, on the rates of wild meat sales and the implications of used to estimate the total biomass and individuals sold in Mod- these meat sales for sanitary risks. These results can inform elo market in that year. decision-making regarding the future of wild meat markets in The same team using the same methods performed all sur- the Amazon and improve understanding of the health and con- veys. The method consisted of market vendors participating servation implications of these markets. willingly in the survey. Vendors fully understood the study and were confident in their anonymity. To engage vendors and encourage participation, preliminary visits to the markets were METHODS made during the first 2 months before each survey period. Because mammals make up 70–80% of all wild meat traded in Study area the Amazon (El Bizri et al., 2020), we focused on this group only. To gather information on the amounts and prices of This study was conducted in Iquitos, the largest city in the Peru- traded wild meat, we used structured interviews and observa- vian Amazon, which had a population of 486,338 inhabitants in tion of meat presented on the counter and stored in the stall. 2018 (Gobierno Regional de Loreto [GOREL], personal com- Team members and local students conducted interviews and munication). In this region, there are few roads, and products, responses were validated with observational information. We including wildlife products, are mainly transported from rural followed the ethical-human-subject guidelines in Buppert and to urban centers through fluvial passage. Iquitos has two large McKeehan (2013). Interviewees were made comfortable with open markets: Belén, which is one of the most important wild our research process by informing them of the study aims prior meat markets in Amazonia in terms of amounts traded, and to the interview and by assuring them that all data would be Modelo, which is a secondary urban market (Bendayan, 1991; anonymous. Respondents were free to participate or not. All Bodmer & Pezo, 2001). Both markets offer many types of goods regular vendors and a large number of occasional vendors of extracted from the rainforest, from traditional medicines and wild meat agreed to participate (5–10% of occasional sellers pets to fish, fresh fruits, and vegetables. declined to participate). Survey questions are provided below. Most wild meat is sold openly in these two markets, making In the 2006–2018 surveys, the average monthly frequency it relatively easy to track. Because the legislation on wild meat of interviews was 9.9 (SD 4.9, range 2.7–15.0), which is above trade is not enforced and the traditional culture of consuming the minimum sampling effort of two interviews/month recom- wild meat is supported by the general public, there is no need mended to obtain proper accuracy and precision in wild meat for a hidden trade and these two markets offer a good proxy for sales and price estimations (Mayor et al., 2019). Interviews were the general consumption of wild meat in Iquitos. Wild meat is conducted daily from 0600 to 1200. The date, species, type of typically supplied by intermediaries, loggers, or by rural hunters, meat preservation (fresh, salted, or smoked), selling price per who travel to the cities to sell products directly to market ven- kilogram, amount of wild meat brought by sellers at the start of dors, who then sell the wild meat from individual stalls in urban the day, including the amount of wild meat displayed on the stall markets (Mayor et al., 2019). and stored indoors, and the amount left at the end of the day were recorded. The amount of wild meat sold was calculated as the difference between the amounts on sale at the beginning Data collection minus the amount left at the end of the day. We avoided double counting of meat brought out again the next day. We used data from seven surveys conducted from 1973 to 2018 We counted the number of species sold at each market and (Appendix S1). Data for 1973, 1986, and 1987, 1996, and 2001 listed them by threat category according to the International 4 MAYOR ET AL. Union for Conservation of Nature (IUCN) (2020). Unidenti- Statistical analyses fied species were grouped by genus and their threat category was filled in by identifying the most likely species traded within We used generalized additive (GAMs) and linear models the genus. (GLMs) to assess temporal trends in wild meat amount, num- The amount of salted and smoked meat recorded per species ber of individuals, species richness, and average body mass of was transformed into fresh meat based on the conversion taxa traded from 1973 to 2018; the relationship between body indices proposed by Bardales-García et al. (2004). For those mass and the amount of fresh wild meat and number of individ- species for which there were no conversion indices, we applied uals traded per taxon (transformed to a log scale) and whether the index for a taxonomically related species of similar body this relationship was similar among years; and the relationship mass. The number of traded individuals per species was esti- between GDP per capita in Iquitos and ICPC of all domestic mated by dividing the amount of fresh meat by the body weight meat pooled. All models were conducted using the Gaussian estimates after evisceration following the calculation proposed family of distribution. We used analysis of variance (ANOVA) by Bardales-García et al. (2004). Both estimations were extrap- to assess differences between the price of meat and survey olated to 365 days to calculate the fresh wild meat biomass and year, preservation type and species (considering only repeated number of individuals traded annually. Species’ body masses species in all surveys). Post hoc differences were tested using were obtained from Peres and Dolman (2000) and Bardales- the Tukey–Kramer multiple comparisons test. A chi-squared García et al. (2004). The estimated average body mass of species test was used to compare percentages of different types of meat sold annually was calculated following the equation Σ (species’ preservation in different years. We also calculated the percent- body mass * number individuals per species)/total number of age, ICPC, and difference of prices of wild meat relative to the individuals of all species sold. total amount of meat consumed in Iquitos from 2000 to 2018 Sellers were asked about the daily amount of wild meat (period for which data on human population and consumption sold, the money spent on purchases to obtain wild meat from of domestic meat were available). In the results, we report the intermediaries or hunters, and the daily sale price per kilogram coefficient estimates of the GAMs and GLMs, which are the of wild meat. Prices of all domestic meat products came from values used to multiply the predictor variables in the models. interviews conducted by the local government employees from These values determine how many units the response variable 2006 to 2018 (GOREL, personal communication). During increases or decreases as the predictor variable is increased by the survey conducted in 2017 and 2018, we interviewed local 1 unit. Statistical analyses were performed using R-Studio ver- sellers to calculate the average daily price per kilogram of meat sion 0.98.1062 (RStudio Inc.) with lme4 and mgcv packages and for all domestic species and the most frequently traded fish, Deducer JRG version 1.7.9.2003-2011 (RoSuDa, University of Prochilodus nigricans. All prices were converted to U.S. dollars Augsburg). based on exchange rates from 10 October 2007 (PS3.00 = US$1.00), 4 July 2014 (PS3.28 = US$1.00), and 4 October 2018 (PS3.32 = US$1.00). We corrected prices based on the Peru- RESULTS vian yearly rate of inflation (https://datos.bancomundial. org/indicador/FP.CPI.TOTL.ZG?end=2017&locations= Trends of wild meat sales PE&start=1993). The amount of wild meat biomass sold from 1973 to 2018 increased significantly at a rate of 6.4 t/year (estimate = 6.4 [SE Economic and demographic drivers of wild 2.17], t = 2.94, p = 0.032) (Figure 1a & Table 1). The number of meat consumption individuals traded also increased over time, but not significantly, likely because of the high number of primate individuals sold in We used the total human population, per capita GDP, annual 1973 (480 individuals that year) (estimate = 0.48, t = 1.86, p = production and prices of meat of domestic animals and fish 0.12) (Figure 1b & Table 1). Belén Market accounted for 65.2– landing rates (GOREL, personal communication) in Iqui- 68.2% of the total biomass sold, and the Modelo Market made tos from 2000 to 2018 in our estimates of meat and fish up the difference. consumption. The index of domestic meat and fish consump- An average of 15 (SD 3.5) taxa of wild mammals was sold tion per capita (ICPC) was calculated by dividing the overall in Iquitos from 1973 to 2018, a decrease over time in the rich- amount of meat produced (for domestic species) or fish landed ness of taxa sold (rate of decrease 0.17 species/year) (estimate annually and daily by the number of inhabitants in Iquitos from = −0.17 [SE 0.06], t = −2.85, p = 0.036) (Figure 1c). In all sur- 2000 to 2018. A similar index of wild meat consumption per veys from 1973 to 2018, Artiodactyla was the most traded order capita considered the overall amount of wild meat sold annually in terms of biomass (70.5% [SD 11.7]) and individuals (52.7% and daily by the number of inhabitants. Data were expressed in [14.7]), followed by Rodentia (25.7% [9.6] of biomass traded and terms of grams per inhabitant per year and grams per inhabitant 44.6% [14.5] of individuals traded) (Table 2). Large numbers of per day. These indices were used to describe temporal trends in primates were sold in 1973 (six species, 12.7% biomass sold). meat consumption and to estimate the relative importance of Primates were prohibited from market sale and excluded from wild meat for the urban population. the list of permitted subsistence species in the 1976 wildlife law, CONSERVATION BIOLOGY 5 FIGURE 1 Trends in trade of wild meat in Iquitos from 1973 to 2018: (a) overall biomass, (b) overall number of individuals, (c) number of different species, (d) average body mass, and (e) biomass and (f) number of individuals of species sold the most (shaded areas, 95% confidence intervals) FIGURE 2 Association between body mass and (a) amount of fresh meat traded and (b) number of individual wild mammals sold in Iquitos from 1973 to 2018 (shaded areas, 95% confidence intervals) 6 TABLE 1 Kilograms of meat of wild mammals and number of individuals (in parentheses) sold per year in Belén and Modelo markets in Iquitos based on data from literaturea (1973, 1986, and 1987, 1996, and 2001 and 2002) and from our surveys in 2006 and 2007, 2013 and 2014, and 2017 and 2018 Year and market sampled 1986 and 2006 and 2013 and 2017 and 1973c 1987 1996 2001 and 2002 2007 2014d 2018 Yearly average kg (%) [SD] Body Meat Species (threat mass mass Belén and Belén and Belén and Belén and Belén and category)b (kg) (kg) Belén Modelo Modelo Modelo Modelo Belén Modelo Biomass Individuals Alouatta seniculus (LC) 6 4 2736 (648) 7.2 (1.8) 19 (4.8) 168 (42) 947 (236) 192 (48) 40 (10) 587.18 [1003.0] (0.3 146.8 [250.8] (0.6 [1.2]) [0.7]) Ateles spp. (VU-EN) 9 6.6 1253 (190) 163 (25) 34 (5.2) 831 (126) 145 (22) 217 (33) 498 (83) 456.0 [447.7] (0.2 [0.3]) 69.1 [67.8] (0.3 [0.3]) Cebus albifrons (LC) 3.5 2.1 912 (434) 0 (0) 0 (0) 0 (0) 0 (0) 0 (0) 0 (0) 182.4 [407.9] (0.1 [0.2]) 108.6 [217.1] (0.3 [0.8]) Coendou sp. (DD-LC) 3.5 2.1 252 (120) 0 (0) 0 (0) 0 (0) 0 (0) 0 (0) 0 (0) 50.4 [112.7] (0.0 [0.1]) 30.0 [60.0] (0.1 [0.2]) Cuniculus paca (LC) 8 6 26,640 10,876 15,397 91,950 (15,325) 83,264 63,310 162,753 64,884.5 [53,974 (22.7 10,515.7 [8378.0] (38.6 (4440) (1812) (2566) (13,877) (10,552) (25,037) [9.4]) [15.6]) Dasyprocta fuliginosa (LC) 5 2 4194 (2097) 516 (258) 219 (110) 705 (325) 329 (164) 0 (0) 73 (36) 862.3 [1489.4] (0.6 [1.1]) 431.1 [744.7] (2.4 [3.6]) Dasypus spp. (LC) 6 4 874 (218) 130 (32) 187 (47) 3325 (831) 2285 (571) 1468 (367) 763 (186) 1290.3 [1167.4] (0.5 321.9 [292.2] (1.2 [0.8]) [0.3]) Didelphis marsupialis (LC) 3 1.8 0 (0) 0 (0) 8.3 (4.6) 0 (0) 0 (0) 0 (0) 0 (0) 1.4 [3.4] (0.0 [0.0]) 0.9 [2.1] (0.0 [0.0]) Hidrochaeris hidrochaeris (LC) 30 12 864 (72) 1323 (110) 1975 (164) 540 (45) 24,917 0 (0) 7132 (554) 6035.2 [9587.2] (1.8 431.8 [748.3] (1.7 [2.3]) (2076) [2.7]) Lagothrix spp. (VU) 11 8 14,302 418 (52) 1176 (147) 3974 (497) 2442 (305) 338 (42) 526 (66) 3311.0 [5025.4] (1.9 413.9 [628.2] (1.9 [2.9]) (1788) [3.5]) Mazama americana (DD) 20 13.7 23,677 3048 (218) 8149 (582) 14,974 (1069) 20,836 0 (0) 27,720 14,058.0 [10,643.7] (6.1 1000.7 [750.7] (4.1 [2.4]) (1691) (1488) (1932) [5.0]) Mazama nemorivaga (DD) 17 11 0.0 (0.0) 0.0 (0.0) 1195 (109) 0 ( 0) 3207 (292) 0 (0) 42 (4) 711.9 [1187.3] (0.2 [0.4]) 90.6 [120.6] (0.3 [0.4]) Mazama spp. (DD-LC) 18.5 1.25 0.0 (0.0) 0.0 (0.0) 0 (0) 0 (0) 7177 (574) 23,983 0 (0) 6232.1 [10,398.4] (1.7 623.2 [905.1] (1.7 [3.2]) (1919) [3.6]) (Continues) MAYOR ET AL. CONSERVATION BIOLOGY TABLE 1 (Continued) Year and market sampled 1986 and 2006 and 2013 and 2017 and 1973c 1987 1996 2001 and 2002 2007 2014d 2018 Yearly average kg (%) [SD] Body Meat Species (threat mass mass Belén and Belén and Belén and Belén and Belén and category)b (kg) (kg) Belén Modelo Modelo Modelo Modelo Belén Modelo Biomass Individuals Myoprocta pratti (LC) 5 2 0.0 (0.0) 1.8 (0.9) 0 (0) 0 (0) 10 (5) 0 (0) 32 (16) 8.8 [13,6] (0.0 [0.0]) 4.4 [6.8] (0.0 [0.0]) Nasua nasua (LC) 5 3 0.0 (0.0) 50 (17) 28 (9.3) 168 (56) 34 (11) 0 (0) 0 (0) 40.0 [59,8] (0.0 [0.0]) 15.8 [20.9] (0.1 [0.1]) Pecari tajacu (LC) 25 13 36,366 33,290 73,291 149,454 (11,496) 101,647 132,872 152,658 97,082.6 [50,752.7] (39.8 7128.2 [3559.2] (32.3 (2797) (2561) (5638) (7.819) (10,221) (9365) [10.7]) [11.9]) Pithecia sp. (DD-LC) 3.5 2.1 648 (309) 0 (0) 0 (0) 0 (0) 0 (0) 0 (0) 0 (0) 129.6 [289.8] (0.1 [0.2]) 77.1 [154.3] (0.2 [0.5]) Potos flavus (LC) 5 3 4716 (1044) 2.6 (0.9) 5.2 (1.7) 0 (0) 0 (0) 0 (0) 0 (0) 523.4 [1278.2] (0.3 [0.8]) 174.5 [426.1] (0.7 [1.8]) Proechimys spp. (DD-LC) 2 1.2 4716 (3930) 0 (0) 0 (0) 0 (0) 0 (0) 0 (0) 0 (0) 943.2 [2109.1] (0.5 [1.2]) 982.5 [1965.0] 82.6 [7.0]) Sapajus apella (LC) 3.5 2.1 864 (411) 0 (0) 0 (0) 0 (0) 38 (17) 0 (0) 0 (0) 180.4 [382.4] (0.1 [0.2]) 107.0 [203.1] (0.3 [0.7]) Tamandua tetradactyla (LC) 7 4.2 315 (75) 76 (18) 17 (3.9) 0 (0) 0 (0) 0 (0) 0 (0) 68.0 [124.5] (0.0 [0.0]) 16.2 [29.7] (0.1 [0.2]) Tapirus terrestres (VU) 140 90 2493 (28) 4692 (52) 8499 (94) 22,290 (248) 12,799 (142) 17,979 (200) 10,565 (109) 11,331.0 [7038.6] (4.8 124.8 [78.4] (0.6 [0.3]) [2.3]) Tayassu pecari (VU) 35 20 18,352 (918) 10,641 90,211 38,913 (1946) 63,404 5052 (253) 79,125 43,671.3 [34,298.9] (17.9 2079.3 [1608.1] (10.2 (532) (4510) (3.170) (3227) [13.2]) [10.2]) Trichechus inunguis (VU) 400 240 1732 (7) 9 (0.04) 0 (0) 0 (0) 93 (0) 0 (0) 0 (0) 366.9 [764.4] (0.2 [0.4]) 1.5 [3.2] (0.0 [0.0]) Total 144,325 65,237 200,411 327,293 (32,061) 323,576 245,412 441,977 249,748.5 [126,506.8] 24,007.1 [11.768.0] (100) (21,246) (5692) (13,997) (30,772) (23,634) (40,647) (100) a Sources: 1973 Castro et al. (1976), 1986 and 1987, Bendayan (1991), 1996 Bodmer and Pezo (2001), and 2001 and 2002 Bendayan and Bardales (2004). b Threat categories according to International Union for Conservation of Nature 2020: DD, data deficient; LC, least concern; VU, vulnerable; EN, endangered. c Local markets included the large market of Belén and two minor markets (Arequipa and Central). Modelo market did not exist at the time. d Modelo market was not surveyed in 2013 and 2014, but we estimated total amount of meat based on the average representativeness of the wild meat amount traded in these markets (33.3% and 66.7% in Modelo and Belén markets, respectively). 7 8 MAYOR ET AL. TABLE 2 Kilograms of fresh meat of wild mammalsa and number of individuals by taxonomic order sold in local markets in Iquitos from 1973 to 2018. Numbers in parentheses are the percentages of each order within each year Artiodactyla Rodentia Primates Cingulata Carnivora Total Year 6 species 4 species 4 species 3 species 2 species 19 species Kg body mass (SD) 42.6 (48.2) 12.0 (12.1) 6.1 (3.2) 5.3 (2.1) 4.75 (0.35) 18.89 (30.8) Kg eviscerated mass (SD) 26.8 (31.1) 5.5 (4.7) 4.6 (2.6) 3.3 (1.3) 2.8 (0.2) 11.54 (19.7) Total biomass sold 1973 80,889 (56.0) 36,666 (25.4) 20,715 (14.4) 874 (0.6) 3132 (2.2) 144,325 (100.0) (kg/year) 1986 and 1987 51,672 (79.2) 12,717 (19.5) 588 (0.9) 130 (0.2) 53 (0.1) 65,246 (100.0) 1996 181,345 (90.5) 17,591 (8.8) 1229 (0.6) 187 (0.1) 33 (0.0) 200,411 (100.0) 2001 and 2002 226,171 (69.1) 92,655 (28.3) 4974 (1.5) 3325 (1.0) 168 (0.1) 327,293 (100.0) 2006 and 2007 209,071 (64.6) 108,520 (33.5) 3573 (1.1) 2285 (0.7) 34 (0.0) 323,576 (100.0) 2013 and 2014b 179,887 (73.3) 63,310 (25.8) 748 (0.3) 1468 (0.6) 0 (0.0) 245,412 (100.0) 2017 and 2018 270,109 (61.1) 169,990 (38.5) 1115 (0.3) 763 (0.2) 0 (0.0) 441,977 (100.0) Total individuals sold 1973 5434 (25.6) 10,659 (50.2) 3816 (18.0) 219 (1.0) 1044 (4.9) 21,247 (100.0) (ind./year) 1986 and 1987 3363 (59.1) 2182 (38.3) 79 (1.4) 32 (0.6) 18 (0.3) 5691 (100) 1996 10,934 (78.1) 2840 (20.3) 157.0 (1.1) 47 (0.3) 11.1 (0.1) 13,997 (100.0) 2001 and 2002 14,822,7 (46.2) 15,723 (49.0) 665 (2.1) 831.3 (2.6) 56.0 (0.2) 32,061 (100.0) 2006 and 2007 13,486 (43.8) 16,123 (52.4) 581 (1.9) 11 (0.0) 11 (0.0) 30,772 (100.0) 2013 and 2014b 12,592 (53.3) 10,552 (44.6) 123 (0.5) 367 (1.6) 0.0 (0.0) 23,634 (100.0) 2017 and 2018 14,638 (36.0) 25,644 (63.1) 159 (0.4) 186 (0.5) 0 (0.0) 40,647 (100.0) a The orders Sirenia, Didelphimorphia, and Pilosa are not included here due to their low representativeness (<0.1%). b The Modelo market was not surveyed in 2013 and 2014, but we estimated total amount of meat considering the average representativeness of the wild meat amount traded in these markets (33.3% and 66.7% in Modelo and Belén markets, respectively). and, more recently, excluded as sustainably hunted species in kg, 17.9%). Red and grey brocket deer were also frequently sold community wildlife plans. From 1987 onward, the trade of pri- (27,762 kg, 8.0% [4.3]) (Table 1). mate meat diminished sharply, decreasing to 0.8% of the overall Five Vulnerable species, woolly monkey (Lagothrix spp.), spi- biomass traded in 2013 and 2014, and 2017 and 2018. der monkey Ateles spp., white-lipped peccary, and lowland tapir Taxa with large body masses were usually sold in larger quan- (Tapirus terrestris), accounted for 5.6% (SD 4.2) of individuals tities than small species, both in terms of biomass (spline term sold (range 1.8–11.1%). Prior to 2006, primates represented = 3.21, F3.63 = 19.73, p < 0.001) and individuals (spline term = 72.8% (17.8) of threatened taxa sold. From 2006 onward, 3.26, F3.67 = 13.15, p < 0.001), but with a decrease in quantities white-lipped peccary and tapir were uplisted to Vulnerable and sold for taxa with body mass higher than 100 kg (Figure 2). An accounted for 91% of threatened taxa (75.9% [24.4] and 15.0% inverted U-pattern described the temporal trend in the average [19.8], respectively), and primates decreased to 9.2% (5.0). body mass of species sold (Figure 1d) (polynomial estimate 1 = There was no significant difference between survey year and 1.91, polynomial estimate 2 = −8.68 [SE 3.00], t = −2.9, p = type of meat preservation (χ2 = 24, df = 22, p = 0.3472). 0.04) and was due to an increase in the average body mass of Smoked wild meat represented 54.1%, 53.5%, and 56.0% of species sold from 1973 to 2002 and the decline of the sales of the biomass sold in 2006 and 2007, 2013 and 2014, and white-lipped peccary (Tayassu pecari) in 2014. 2017 and 2018, respectively. In these same years, salted wild Five taxa made up 88.5% (SD 7.6) of the total biomass sold meat accounted for 31.4%, 32.5%, and 40.0% and fresh meat in all years (Figures 1e,f): paca (Cuniculus paca), collared peccary accounted for 14.5%, 14.0%, and 4.0% of biomass sold, respec- (Pecari tajacu), white-lipped peccary, and red (Mazama americana) tively. and grey (Mazama nemorivaga) brocket deer. The collared peccary was the most frequently sold taxon in terms of biomass (39.8% [10.7]) and the second most sold in terms of individuals (32.3% Economic value of wildlife [11.9]). The paca was the most commonly sold taxon in terms of individuals (38.6% [15.6]) and the second most sold in terms of From 2006 to 2018, consumers spent US$1,053,851 (2006 and biomass (22.8% [9.4]). White-lipped peccary sales crashed in the 2007), US$1,217,673 (2013 and 2014), and US$2,591,591 (2017 2013 and 2014 survey, going from the most commonly sold wild and 2018) on wild meat in the markets of Iquitos. Taking into meat in 1996 (90,211 kg, 45.0%) to virtually disappearing from account yearly inflation, wild meat presented a similar economic the urban markets in 2014 (5052 kg, 2.1%). As white-lipped pec- benefit for the regional economy from 2006 and 2007 to 2013 cary sales declined, paca sales increased. In 2017 and 2018, the and 2014 (US$1,053,850 and US$999,223, respectively), but trade in white-lipped peccary showed signs of increasing (79,125 showed a growth of 92.0% in 2017 and 2018 (US$1,918,972). CONSERVATION BIOLOGY 9 TABLE 3 Average prices (in US$) per type of meat, including domestic and wild meat and fish, in Iquitos during the surveys conducted in 2006 and 2007, 2013 and 2014, and 2017 and 2018 Local average Difference prices (SD) compared with Official average prices (USD/kg)a Price difference between years (%) (US$/kg) wild meat (%) 2006 2013 2017 and and and 2014 versus 2018 versus 2018 versus Meat type 2007 2014 2018 2007 2014 2007 2017 and 2018 Poultry 1.93 2.38 2.21 23.2 –7.2 14.4 3.14 (0.32) 45.8 Regional hen 3.65 3.66 4.01 0.3 9.7 10.0 – – Pork 1.50 1.55 2.14 3.5 37.6 42.4 4.36 (0.22) 24.7 Beef 2.07 1.37 1.66 –33.6 20.7 –19.8 4.81 (0.23) 16.9 Total 2.29 2.24 2.50 –2.2 11.6 8.4 4.10 (0.76) 29.2 domestic meat Fish – – – – – – 3.06 (0.17) 47.1 Wild meat 2.88 4.26 5.79 47.9 35.9 101.0 5.79 (0.24) 0.0 a Official average prices of domestic animals (poultry, pork, and beef) were obtained from the Dirección Regional de Agricultura de Loreto (personal communication). The price was significantly influenced by the year, taxon, and type of meat preservation; the interaction between taxon and type of meat preservation was significant (F15,8487 = 8.24, p < 2.2e-16). The average selling price of wild meat grew by 101.0% from US$2.88/kg (SD 0.25) (2006 and 2007) to US$4.26/kg (0.93) (2013 and 2014) and to US$5.79/kg (0.74) (2017 and 2018) (F2,8487 = 9739.1, p < 0.001) (Table 3). Paca was the most expensive meat (F8,8496 = 715.7, p < 0.001), followed by brocket deer and peccaries; tapir and primates were the least expensive. Preservation method also affected the price (F2,8502 = 22.97, p < 2.2e-16); salted meat was less expensive than smoked and fresh meat. The money spent by sellers to obtain wild meat from intermediaries and hunters decreased 9.9%, from US$2.21/kg (0.60) in 2006 and 2007 to US$1.91/kg (0.23) in 2017 and 2018. The increase in sale prices and the decrease in purchase price resulted in an increase in average profit per kilogram of wild meat of 214.1% for vendors: 30.3% (2006 and 2007) to 67.0% (2017 and 2018). In parallel, prices of domestic meat showed a moderate increase of 8.4% from 2006 and 2007 to 2017 and 2018. Poul- try, the most purchased meat, increased in price by 14.4%, from US$1.93 (2006 and 2007) to US$2.21 (2017 and 2018). In 2017 and 2018, wild meat was the most expensive meat; average price was 47.1% higher than the most frequently consumed fish, P. nigricans, 45.8% higher than poultry, 24.7% higher than pork, and 16.9% higher than beef. FIGURE 3 Trends in consumption of (a) overall animal protein (ICPC) Demographic drivers and per capita relative to per capita gross domestic production (GDP) and (b) of domestic consumption of wild meat meat and fish (Dirección Regional de Agricultura de Loreto, personal communication) and fish (Dirección Regional de la Producción de Loreto, The ICPC of wild meat in Iquitos remained low and relatively personal communication) in Iquitos during from 2001 to 2015 (total includes domestic meat, fish, and meat of wild mammals) (shaded area, 95% confidence constant over the years (1.99 g/inhabitant/day [SD 0.49], t = interval) 0.60, p = 0.58); minimum and maximum rates were 435 and 10 MAYOR ET AL. 926 g/inhabitant/year (1.0 and 2.5 g/inhabitant/day) in 2013 International Trade in Endangered Species of Wild Fauna and and 2014, and 2006 and 2007, respectively. Wild meat repre- Flora in 1973. In addition, the transient decrease in sales in sented only 3.2% of total meat consumed in 2001 and 2002, 2013 and 2014 is likely explained by ecological factors. In the and its contribution decreased to 0.7% (2013 and 2014) and flooded forests of Loreto, the extreme floods of 2011−2015 0.9% (2017 and 2018). From 1973 and 2018, the human pop- caused large-scale die-offs of game species. Consecutive nor- ulation in Iquitos grew from 182,738 to 486,338. The GDP per mal floods from 2016 to 2018 allowed their population recovery capita showed an average yearly increase of 8.5% (7.6) from (Bodmer et al., 2020). Nevertheless, we must be cautious with US$2,016 (2001) to US$6,177 (2015). The overall consumption that estimate because Modelo market was not surveyed in 2013 of animal protein grew 6.9%, from 82.1 (2000) to 240.7 (2018) and 2014. g/inhabitant/day. Amazonian people have traditionally used different subsis- Gross domestic product per capita and the ICPC of all meat tence resources, such as fish and wild meat. More recently, pooled were highly associated (estimate = 0.026 [SE 0.003], local inhabitants have adjusted their diets to include meat from t = 7.96, p < 0.001) (Figure 3a). The daily consumption of domestic species, and wild meat is transitioning from a tra- domestic species increased from 56.3 (2000) to 215.1 (2018) ditional dietary component to a complementary and expen- g/inhabitant/day, an average yearly increase of 8.1% (SD 8.7). sive but still relatively affordable meat. Simultaneously, the rise Poultry was the most consumed meat, and daily consump- of domestic meat production, especially the poultry industry, tion increased yearly by 8.2% from 49.4 (60.2% of total meat) has resulted in higher consumption of protein from domes- g/inhabitant/day in 2000 to 192.9 (80.1%) g/inhabitant/day tic species. From 2001 to 2014, poultry production grew by in 2018 (Figure 3b). Although the daily consumption of fish 284% and comprised 76% of the total daily meat intake. In con- remained constant, its dietary contribution decreased from trast, the improvement of local economies did not result in an 31.4% to 10.6%. Daily consumption of sheep, buffalo, pork, and increase in the proportion of wild meat traded among all avail- beef showed a yearly increase of 21.6%, 15.7%, 9.9%, and 5.9%, able meat; meat sales maintained low levels (<2% of total meat respectively, but their contribution to overall meat consumption traded). The higher price of wild meat compared with that of was low (≤ 5%). fish (+47%) and poultry (+45%) likely contributed to restrict- ing its accessibility. Based on the optimal foraging theory, hunters should har- DISCUSSION vest the most profitable and largest prey available (Hawkes et al., 1982). Accordingly, we found that species with relatively The emergence of the COVID-19 pandemic initiated substan- high body mass were generally traded more often. However, we tial global political and economic changes and brought about detected an inverted U-shaped curve in the amount of meat and one of the main challenges humanity has ever faced with links individuals traded caused by the tapir and manatee (Trichechus to loss of biodiversity and human health and food security. Our inunguis). Although tapir and manatee are among the largest and results provide fundamental information for decision makers more profitable species due to their large size and high amounts regarding the sustainability and risks posed by trade of wild of meat, these species are less dense and therefore more diffi- meat. With 45 years of data, we were able to assess trends and cult to catch in the forest, making them slightly less prevalent the economic and sociocultural drivers of wild meat trade in in the market than expected based on body mass. Tapir is in Amazonia. less demand due to its dark, oily meat, which is less preferred The population of Iquitos has been rising 1.3%/year. This by consumers. In 1973, this trend was not clear, mainly because increase is due to both population growth and urban migra- of the high numbers of primates sold, which likely reflect a cul- tion. Thus, over the last five decades, overall wild meat sales tural preference for these species 45 years ago. As reported in in urban markets have increased, although ICPC remained con- other studies in the Amazon (van Vliet et al., 2014; El Bizri et al., stant. The inclusion of new technologies and transportation has 2020), ungulates and rodents accounted for 90% of the amount enhanced the capacity of hunters to capture prey, even in previ- of biomass of mammals traded in the Iquitos markets. The most ously inaccessible areas (Chaves et al., 2017; Bowler et al., 2020). frequently sold species, the collared peccary and the paca, are However, in contrast to what we expected based on the find- less vulnerable to overhunting and more likely to be used as a ings from the Brazilian Amazon (Chaves et al., 2020), we did source of wild meat due to their large population size and rel- not find evidence of a decrease in wild meat consumption over atively fast reproductive rates (Mayor et al., 2017). Accordingly, generations. Even if ICPC were to remain constant, the overall creation and reinforcement of management strategies to ensure sustainability threshold could be exceeded because of the con- these species are hunted sustainably are needed. The Peruvian stant increase in the urban population. This scenario needs con- Forestry and Wildlife Service has an annual subsistence hunting sideration, and addressing the problem would require regulating quota for peccaries because pelts originating from subsistence all traded species, even nonthreatened ones, in order to ensure hunters are sold on the international market in accordance with long-term sustainability. CITES II regulations (Fang et al., 2008). There is no annual sub- Despite the increasing trend of the trade in wild meat, sistence hunting quota for paca, whose pelts are not traded. decreased levels of trade were recorded in the survey period. The low presence of species threatened with extinction in the Results from the survey conducted in 1987 probably reflect the markets suggests that the trade exerts mild pressure on species regulatory effect of the implementation of the Convention on of high conservation concern, which mainly comprise taxa with CONSERVATION BIOLOGY 11 low reproductive rates, such as primates and tapir (Mayor et al., emergence of COVID-19 has put wild meat at the center of this 2017). We observed a significant decrease in the sale of primate discussion. In Amazonian markets, wild meat and animals are meat over time, possibly because of a greater stigma associated often stored for sale in open-air settings and in close proximity with consumption of primates due to their taxonomic proxim- to domestic meat, which breaches health sanitation standards. ity to humans and their human-like appearance (Lemos et al., The main route for contamination by foodborne pathogens in 2021). The presence of primates in the markets in Iquitos is wildlife markets is through direct contact with vectors or body low compared with the numbers hunted in rural areas (Mayor fluids of animals, handling of carcasses, and ingestion of raw et al., 2015). However, hunting and trade combined may com- or undercooked meat (van Vliet et al., 2017). Moreover, in the promise primate populations (Pérez-Peña et al., 2018). Further- tropics, the presence of high levels of nutrients, in combination more, primates may be important hosts for emergent viruses of with high humidity, plays an essential role in the proliferation pandemic potential, increasing the chances of disease spillover and survival of microorganisms in the meat and on wood sur- from animals to humans (Johnson et al., 2020). The best mea- faces (Carpentier, 1997). sure for safeguarding primate conservation and public health is These conditions are common in markets throughout trop- to continue the prohibition of primate meat sales in the mar- ical forests worldwide. Existing global food-safety regulations kets and to continue to exclude primates from sustainable-use have helped improve hygienic practices and hazard analysis at wildlife management plans. critical control points for safer processed foods (Mahajan et al., The amount of money spent by consumers provides an esti- 2014). However, these are not frequently implemented in tra- mate of the economic value of wild meat in urban centers (Bod- ditional wildlife markets, thereby causing food-safety concerns mer & Pezo, 2001). The revenue from wild meat sales reached (Blanck et al., 2014). To the best of our knowledge, the only US$2.6 million in 2018, when it contributed 0.76% to the total microbiological study conducted for wild meat in the markets of GDP of the Loreto region (US$34,340 million). Compared with Iquitos showed high contamination levels (Lozano et al., 2014); other commercial activities, wildlife sales make up a relatively however, similar results were found for domestic meat (Soplin & low proportion of the total GDP (oil industry 81.1%, fish- Tulumba, 2013), demonstrating general deficiencies in hygiene eries 6.9%, agriculture 5.7%, and timber industry 4.6% [DDPI– practices. Mincetur, 2018]). Unlike other activities, the harvest and trade The meat preservation methods of salting, drying, and smok- in wildlife does not generate longstanding socioenvironmental ing have a long tradition. In Iquitos, 85% of wild meat is sold conflict (Yusta et al., 2017). Trade in wild meat in Iquitos has smoked or salted, which reduces sanitary risks. Fresh carcasses the potential to increase the economic returns for local people. are more likely to be contaminated with a variety of microorgan- However, although urban vendors optimized their economic isms (Alekruse et al., ). A range of pathogens are susceptible to performance, with a 55% increase from 2006 to 2018, there changes in temperature, pH, relative humidity, and time. Many was no similar economic incentive for rural people to partici- viruses may be deactivated when exposed to 60◦ C temperatures pate in the trade (their profits decreased by 10%). Because urban for 60 min (e.g., coronaviruses [Hessling et al., 2020]). Smoked sale of wild meat is mostly illegal, it is excluded from official meat is usually cooked to 65−75◦ C, a temperature sufficient to statistics. This hampers tracking of the actual economic value destroy most vegetative microorganisms, but not thermoduric of wildlife, which is why wildlife specialists have been collecting enterococci and bacterial sporeformers (Cerveny et al., 2009). market sales intermittently over the past 45 years. The salting process in dry curing reduces the amount of water Low livestock productivity in the Afrotropics makes wild available for microbial growth (Scolari et al., 2003). Thus, proper meat hunting one of the more profitable rural economic activ- salting and smoking should significantly reduce sanitary risks. ities in this region (Milner-Gulland et al., 2002). In contrast, However, further studies into this subject are needed. as reported across the Amazon basin (Oestreicher et al., 2020; It has been suggested that banning the trade of wild meat Chaves et al., 2020), in Iquitos, the increasing availability of could reduce the risk of future pandemics. However, this is a cheaper sources of animal protein, such as poultry and fish, complex issue because these markets support informal food sys- appears to have reduced dependence on wild meat. This sug- tems for millions of urban and rural people. The number of gests that economic development may be compatible with game zoonotic viruses in mammalian species is related to a species’ species conservation. As long as strategies to minimize the ability to adapt to human-dominated landscapes; domesticated impacts of harvests on populations are developed, wild meat species, primates, and bats have more zoonotic viruses than may be sustainably used as subsistence food in rural areas other species (Johnson et al., 2020). Local markets involve wild (Bodmer & Pezo, 2001) and as an income source for local peo- and domestic species in close proximity, providing opportuni- ple by acting as a complementary good to domestic meat in ties for pathogens to move between them. Alternatively, the urban areas (Wilkie & Godoy, 2001). For instance, wildlife man- combination of restrictive regulations, creation of management agement plans in Pucacuro National Reserve and the Ampiyacu- strategies that sustain trade in wild meat, and effective edu- Apayacu Regional Conservation Area in the Peruvian Amazon cational programs on appropriate hygiene practices may sus- have been approved that legally permit the sale of wild meat in tain wild meat trade and resolve sanitation problems. As main urban markets for the first time since the ban on the urban wild restrictive measures, we advocate banning trade in live animals meat trade in 1976. and fresh wild meat and that the sale of primate meat remain However, authorities need to consider foodborne diseases prohibited. 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Microbiological spoilage of been possible without the logistical and financial support of the meat and poultry products. Pages-69–86 in Sperber WH, Doyle MP, editors. Center for International Forestry Research (CIFOR-CGIAR- Compendium of the microbiological spoilage of foods and beverages. Springer Nature, USAID-DFID), the Wildlife Conservation Society (WCS), the Switzerland. Earthwatch Institute, the Gordon & Betty Moore Foundation, Chaves, W. A., Wilkie, D. S., Monroe, M. C., & Sieving, K. E. (2017). Market the Iniciativa para la Conservación de la Amazonia (ICAA), access and wild meat consumption in the central Amazon, Brazil. Biological Conservation, 212, 240–248. the World Wildlife Fund (WWF), and the Darwin Initiative, Chaves, W. A., Valle, D., Tavares, A. S., Morcatty, T. Q. & Wilcove, D. S. (2021). UK. 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