Svensson et al. 1 1 Disappearing in the night: an overview on trade and legislation of 2 night monkeys in South and Central America 3 Magdalena S. Svensson1,2, Sam Shanee1,3,4, Noga Shanee3,4, Flavia B. Bannister1, 4 Laura Cervera5,6, Giuseppe Donati1, Maren Huck7,8, Leandro Jerusalinsky9, 5 Cecilia P. Juarez8,10, Angela M. Maldonado11, Jesus Martinez Mollinedo12, Pedro 6 G. Méndez-Carvajal13, Miguel A. Molina Argandoña14, Antonietta D. Mollo 7 Vino14, KAI Nekaris1,2, Mika Peck15, Jennifer Rey-Goyeneche1, Denise Spaan16, 8 Vincent Nijman1,2 9 10 1Nocturnal Primate Research Group, Oxford Brookes University, Oxford, UK 11 2Oxford Wildlife Trade Research Group, Oxford Brookes University, Oxford, UK 12 3Neotropical Primate Conservation, Manchester, UK 13 4Asociacion Neotropical Primate Conservation Peru, Yambrasbamba, Peru 14 5Asociacion Ecuatoriana de Mastozoologia, Quito, Ecuador 15 6Grupo de Estudio de Primates del Ecuador, Quito, Ecuador 16 7Environmental Sustainability Research Centre, University of Derby, Derby, UK 17 8Owl Monkey Project, Formosa, Argentina 18 9Centro Nacional de Pesquisa e Conservação de Primatas Brasileiros, Instituto Chico 19 Mendes de Conservação da Biodiversidade, Brasília, Brazil. 20 10Universidad Nacional de Formosa, Formosa, Argentina. 21 11Fundacion Entropika, Leticia, Colombia 22 12Wildlife Conservation Society, La Paz, Bolivia 23 13Fundación Pro-Conservación de los Primates Panameños, Panama City, Panama 24 14Dirección General de Biodiversidad y Áreas Protegidas, Viceministerio de Medio 25 Ambiente, Biodiversidad, Cambios Climáticos y de Gestión y Desarrollo Forestal. La 26 Paz, Bolivia 27 15University of Sussex, Brighton, UK 28 16Instituto de Neurología, Universidad Veracruzana, Xalapa, México 29 30 Svensson, M.S. (Oxford), Shanee, S., Shanee, N. (Manchester/Yambrasbamba), 31 Bannister, F.B. (Oxford), Cervera, L. (Quito), Donati, G. (Oxford), Huck, M. 32 (Derby/Formosa), Jerusalinsky, L. (Brasília), Juarez, C.P. (Formosa), Maldonado, A.M. 33 (Leticia), Martinez Mollinedo, J. (La Paz), Méndez-Carvajal, P.G. (Panama City), 34 Molina Argandoña, M.A., Mollo Vino, A.D. (La Paz), Nekaris, K.A.I. (Oxford), Peck, 35 M. (Brighton), Rey-Goyeneche, J. (Oxford), Spaan, D. (Xalapa), Nijman, V. (Oxford) 36 37 38 Short title: Trade in Night Monkeys 39 40 Corresponding author: Magdalena Svensson, Oxford Brookes University, Nocturnal 41 Primate Research Group, Oxford OX3 0BP, UK. 42 Svensson et al. 2 43 ABSTRACT 44 International trade in night monkeys (Aotus spp.), found throughout Central and South 45 America, has been regulated through the Convention on International Trade in 46 Endangered Species of Wild Fauna and Flora since 1975. We present a quantitative 47 analysis of this trade from all nine range countries, over four decades, and compare 48 domestic legislation to CITES regulations. Night monkeys were exported from eight of 49 the nine habitat countries, totalling 5,968 live individuals and 7,098 specimens, with 50 trade of live individuals declining over time. In terms of species the most commonly 51 traded was Aotus nancymaae (present in Brazil, Colombia, Peru) followed by A. 52 vociferans (Brazil, Colombia, Ecuador, Peru) and A. zonalis (Colombia, Panama). There 53 was no significant correlation between levels of trade and species’ geographic range 54 size or the number of countries in which a species occurs. Five countries have 55 legislation that meet CITES’ requirements for implementation, whereas the other four 56 countries’ legislation showed deficiencies. Research conducted in Colombia, Peru and 57 Brazil suggests significant cross-border trade not captured in official international trade 58 registers. Although international trade diminished, current trends suggest that 59 populations of rarer species may be under unsustainable pressure. Further research is 60 needed to quantify real trade numbers occurring between habitat countries. 61 62 KEY WORDS: Aotus; CITES; douroucoulis; domestic legislation; malaria research; 63 Neotropics; owl monkeys 64 65 66 Svensson et al. 3 67 INTRODUCTION 68 Primates worldwide are threatened through habitat loss, forest fragmentation, 69 overhunting as well as legal and illegal trade, including the trade for consumption, 70 medicine and as pets [Duarte-Quiroga et al., 2003; Nekaris and Jaffe, 2007; Ceballos- 71 Mago et al., 2010; Nijman et al., 2011; Strier, 2011; Svensson and Friant, 2014; Nijman 72 and Healy, 2016]. Primates are traded domestically, for instance within a village or from 73 one village to the next [Nekaris et al., 2010], regionally, for instance from one province 74 to the next [Shanee et al., 2015b; Nijman et al., 2016], across international borders from 75 one country to the next [Maldonado et al., 2009], and globally, from one continent to 76 another [Mack and Mittermeier, 1984; Nijman et al., 2011; de Souza Fialho et al. 2016]. 77 This trade occurs within and amongst primate range countries and non-primate range 78 countries [Nijman et al., 2011]. While much of the international primate trade follows 79 domestic legislation and international agreements, some of it is illegal [Maldonado et 80 al., 2009; Nijman and Healy, 2016]. Partially due to their cryptic nature, nocturnal 81 species have often been excluded from studies on trade [Nekaris and Nijman, 2013; 82 Svensson and Friant, 2014]. Recent work has, however, found them to be increasingly 83 threatened by both domestic and international trade [Shepherd et al., 2005; Maldonado 84 and Peck, 2014; Nijman and Nekaris, 2014; Svensson and Friant, 2014; Shanee et al., 85 2015b; Svensson et al., 2015]. 86 In assessing the scale and traceability of the trade, the ever-changing taxonomy 87 of many primate taxa is problematic as outdated taxonomies and synonyms lead to 88 difficulties in identifying which species are traded from where [Mace, 2004]. Again, 89 this is especially prominent in nocturnal primates, which have seen significant 90 taxonomical changes as, until recently, their true diversity in terms of number of species Svensson et al. 4 91 has not been recognized [Hershkovitz, 1983; Groves, 2001; Nekaris and Bearder, 2011]. 92 A case in point are the night monkeys (Aotus spp.), also referred to as owl monkeys or 93 douroucoulis. Their range is vast, encompassing the Chaco plains of Argentina in the 94 south to Coclé del Norte in Panama’s rainforests in the north [Fig. 1; Fernandez-Duque 95 et al., 2013]. Since night monkeys were first described in 1802 by Félix de Azara 96 [Goldman, 1914], the taxonomy and suggested arrangements of the number of species 97 and subspecies has been greatly debated [Defler and Bueno, 2007]. Until 1983, when 98 nine taxa were suggested, they were thought to comprise only one species, Aotus 99 trivirgatus [Hershkovitz, 1983]. Here we follow the taxonomy used by Fernandez- 100 Duque et al. [2013], recognizing 11 species, which also coincides with the International 101 Union for Conservation of Nature’s (IUCN) Red List. Five of these are listed as Least 102 Concern on the 2008 assessment (Aotus azarae, A. nancymaae, A. nigriceps, A. 103 trivirgatus and A. vociferans), 4 as Vulnerable (A. brumbacki, A. griseimembra, A. 104 lemurinus and A. miconax) and two as Data Deficient (A. zonalis and A. 105 jorgehernandezi) [IUCN, 2008]. The population trends for all species are either 106 considered decreasing or unknown by the IUCN Red List; none is listed as having 107 stable or increasing population trends [IUCN, 2008]. The population trends for all 108 species are either considered decreasing or unknown by the IUCN Red List, none is 109 listed as having stable or increasing population trends [C. Schwitzer, pers. comm]. 110 111 112 Svensson et al. 5 113 Figure 1. Distribution of Aotus species. AR) Argentina, BO) Bolivia, BR) Brazil, CO) Colombia, EC) 114 Ecuador, PA) Panama, PE) Peru, PY) Paraguay, VE) Venezuela. Map created using IUCN shape files 115 [IUCN, 2008]. 116 117 Like many other primate species, most night monkey species are threatened by 118 varying levels of habitat loss throughout their range, mainly caused by expansion of the 119 agricultural frontier, cattle ranching, logging, armed conflict and mining operations 120 [Butchart et al., 1995; Strier, 2011; Shanee et al., 2015a]. Additionally to these threats, 121 night monkeys have been, and continue to be, traded domestically, regionally and 122 internationally [Mittermeier et al., 1994; Maldonado et al., 2009; Shanee, 2012; Ruiz- 123 García et al., 2013; Shanee et al., 2015b]. 124 In this study we firstly provide an overview of the trade in night monkeys from 125 the 1960s onwards, and secondly we present the results of a quantitative analysis of the 126 international trade in night monkeys from all nine South and Central American range 127 countries. In this analysis we take into account, and explore relationships between, trade Svensson et al. 6 128 volumes, origins and destinations, proportions of live trade, species identity and 129 species’ geographic range size. Finally we provide an overview of the relevant domestic 130 legislation and how well this complies with the rules and regulations of the Convention 131 on International Trade in Endangered Species of Wild Fauna and Flora (CITES), and 132 how this compares to recorded levels of international trade. We hypothesize that the 133 combined effect of legal and illegal trade is a real and emerging threat even for cryptic 134 primate species and we intend this overview document to be available for conservation 135 planning. 136 137 METHODS 138 We downloaded data in October 2016 on the export of night monkeys from the CITES 139 trade database (http://trade.cites.org/) for the period 1975 – 2014 (data from 2015 were 140 not yet available). For four 10-year periods (Table 1) we established the number of live 141 and dead individuals that were exported from range countries as well as the number of 142 specimens. It is possible to overestimate the number of individuals when counting 143 specimens in the CITES database as specimens are defined as any readily recognizable 144 part or derivative of the animal (we use the definition of specimen as described by 145 www.CITES.org).