Hunting pressure on primates in the southern portion of the Brazilian Northeast: historical threats and current perspectives

Hunting is an ancient human behavior, which likely became complex and efficient gradually through time. We present data from a bibliographic survey (qualitative) and field sampling (quantitative) of primate hunting in Northeastern Brazil. We evaluated hunting threats faced by 14 primate species native to the States of Bahia and Sergipe (three Critically Endangered, three Endangered, three Vulnerable, two Near Threatened, and three Least Concern). Qualitatively, since 2005, we identified 21 academic studies that contained 47 mentions of all six studied genera known to occur in the study area ( Alouatta =4, Brachyteles =2, Callicebus =16, Callithrix =8, Leontopithecus =3, Sapajus =14). Approximately half of the citations were for hunting (55.3%; 88.4% of this for bushmeat) and the other half for trapping (44.7%; 90.4% for pet). Quantitatively, we obtained 834 local experts’ citations of primate hunting and capturing at 348 sites. All experts cited Callithrix , 818 cited Sapajus , and 738 cited Callicebus . We argued 539 about hunting for bushmeat (164 positive; 30.4%) and 636 about trapping for pet (189 positive; 30.9%). Callicebus presented 95 citations as bushmeat (30.1% of 326 queries) and Sapajus presented 80 citations as pet (35.7% of 224). Four informants reported hunting Sapajus for pest control because of crop damage. There was a significant difference (Chi²=33.982; df=2; p<0.0001) comparing hunting for bushmeat and pets, with Callicebus (higher bushmeat) and Sapajus (higher pet) presenting significant differences (both p<0.01). The impact of hunting is associated with biological contexts, besides socioeconomic and political, requiring complex-specific attention and efforts in conservation and management strategies, perhaps innovative, even non-prohibitive hunting.


INTRODUCTION
Hunting is an ancient human behavior of unknown origin (Hill 1982), which likely became more complex and efficient quite gradually through time over the course of the evolution of Homo sapiens (Klein 1987).Hunting was important precursor of agricultural practices, contributing to the advancement of human societies (Nitecki 1987), and is still an important component of the subsistence strategies of some human societies (Sponsel 1997;Peres 2001;Nunes et al. 2017).In the present day, however, hunting is second only to habitat loss and fragmentation as a major threat to the planet's terrestrial fauna (Cowlishaw and Dunbar 2000;Benítez-Lopez et al. 2017;ICMBio 2018).
In addition to its impact on populations, which includes local extinction, in some cases, hunting may lead to other processes, such as the loss of genetic variability, key ecological processes, and certain plant species, as well as the homogenization of landscapes (see Redford 1992;Cowlishaw and Dunbar 2000;Tabarelli et al. 2004;Terborgh et al. 2008;Wilkie et al. 2011;Bagchi et al. 2018).Hunting, combined with habitat loss and fragmentation, imposes severe limitations on a local fauna (Novaro et al. 2000), in particular animals, such as Neotropical primates, that are dependent on forest habitats (Gouveia et al. 2014).
In addition to subsistence, hunting has a number of alternative objectives, including the trade in bushmeat and medicinal substances (Stanford 1999;Alvard et al. 1997;Cowlishaw and Dunbar 2000), pest control (King and Lee 1987;Lee and Priston 2005), and sport (Bekoff and Jamieson 1991;Loveridge et al. 2007).Here, we differentiate trapping as the non-lethal harvesting of animals, for the capture of pets or trade, legal or otherwise, although, in the specific case of primates, this may often include the death of certain individuals (Ceballos- Mago et al. 2010).Hunting tends to result in a drastic reduction in population size, as observed in some Neotropical mammals (Robinson and Redford 1991), including many Brazilian primates (Costa et al. 2005;Chiarello et al. 2008;ICMBio 2018).Under certain conditions, hunting may even lead to the local extinction of a primate species (Aguirre 1971;Lane 1990;Cowlishaw and Dunbar 2000).
Under most circumstances, hunting is illegal in Brazil (Brasil 1998), which means that this activity tends to be under-reported in the extreme, although some insights into the illegal trade in wildlife are provided by the monitoring of government agencies.Between 1999 and 2006, for example, the wildlife screening centers (CETAS: Centros de Triagem de Animais Silvestres) of the Brazilian Environment Institute (IBAMA: Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis) documented more than 4,500 primates, derived from actions against illegal trade, confiscations, and donations (Levacov et al. 2011).A total of approximately 1,300 legal trade transactions in Brazilian primates have also been registered since 1977 (Fialho et al. 2016).In fact, considering the trade only for zoos and scientific purposes (between 1977 and 2013), approximately 90,000 live Neotropical monkeys were exported from all South American habitat countries (except Ecuador).During a similar period , night monkeys (Aotus spp.) alone contributed more than 13,000 individuals (Svensson et al. 2016), which were exported from Brazil, Colombia, Ecuador, Panama, and Peru.While striking, it seems likely that these numbers underreport the real scenario considerably.In fact, Maldonado et al. (2009) reported that approximately 4,000 night monkeys (Aotus spp.) were captured or traded from the Brazil-Colombia-Peru border region in 2007 and 2008 alone.
A number of Brazilian primates are under some level of threat of extinction (see Costa et al. 2005;Chiarello et al. 2008;MMA 2014;ICMBio 2018), with the scenario being exacerbated, in many cases, by hunting pressure.This problem is especially intended in eastern Brazil, primarily in the Atlantic Forest and Caatinga domains, which have been subject to the most critical levels of habitat impact (see MapBiomas 2022).In the present study, we review both qualitative (literature search) and quantitative (field sampling) data on the hunting of primates in the southern portion of the Brazilian Northeast region, that is, the states of Bahia and Sergipe.We also applied a quantitative analysis to identify the principal threat faced by each primate genus, considering the focus of the hunting activity affecting each taxon.

Qualitative Data Sampling
We surveyed and assessed the published academic literature and unpublished reports from research projects produced since 1997 up to 2023 that refer to the hunting and trapping of primates within the study area.We search the Web of Science catalogue and Google Scholar using the names (scientific and common names, former and current typos) of all primate species and genus occurring in the study area (see above), followed by the terms "hunt", "hunting", "pet", "pet trade" together with the connectors "or" and "and".We scrutinized the References of the articles and reports we find in order to identify additional documents.These documents were examined to determine the target species and the principal objective of the activity, i.e., hunting or trapping, and the specific subcategories.We also examined the studies to identify the number of citations or hunting events documented for each species, and any other information considered relevant to our goal.

Quantitative Data Sampling
The assessment of the conservation status of a species based on a participative and integrative research depends on the adequate identification of the local residents that are considered to be local experts in their respective communities.In addition, since we knew about the absence of some species at specific sites, we did not argue all the informants comprehensively, thus not arguing about all species or all hunting purposes.Besides, when the needed information is highly sensitive, such as hunting, a practice that is considered illegal in Brazil (Brasil 1998), running the proper research method is crucial to the effectiveness of the survey and assessment.This strategy allowed us to dedicate field effort accurately to sites with a higher probability of occurrence of the assessed primate species or to survey more accurate information concerning its conservation status, besides past and current threats (e.g., Kierulff et al. 2005;Jerusalinsky et al. 2006;Marques et al. 2013a,b;Beltrão-Mendes and Ferrari 2019).
We identified local experts (Davis and Wagner 2003) using a set of approaches, but primarily unprompted and undirected interviews (Chizzotti 2005; Bernard 2011), in particular, by using the snowball technique to identify the most valuable potential interviewer (Goodman 1961;Johnson et al. 1989;Browne 2005;Bernard 2011;Printes 2011).In addition to their knowledge of the local wildlife, it was important to select experienced individuals that were resident in the vicinity of primate habitats, and are or were active in the exploitation of natural resources, in particular, hunting.We used colored plates (Mittermeier et al. 2007;Reis et al. 2015), and recordings of vocalizations (Emmons et al. 1998) to ensure the identification of primate species.The colored plates contained local and autochthonous species to ensure the correct identification of local species by the experts.
The data presented here are derived from previous studies of the distribution and occurrence of primate species in northeastern Brazil (Jerusalinsky et al. 2006;Marques et al. 2013a,b;Beltrão-Mendes and Ferrari 2019;Alonso et al. 2024;Jerusalinsky et al. unpub. data), together with records compiled by the authors of the present study.We surveyed 348 sites, distributed throughout the study area.Whenever the local occurrence of primates was confirmed, we compiled all possible information on the characteristics of the species and the type of exploitation (hunting or trapping, and their respective subcategories).These data were collected as part of a broader survey that focused on the mammalian fauna of the study area as a whole, although only the data on the hunting of primates are presented and analyzed here.

Data analysis
Given the limited database available for some species, the data were analyzed per genus, which is justifiable given the similar characteristics of congeners, in particular in terms of the threats they face (see ICMBio 2018; IUCN 2024).As the assessment is limited primarily by the number of studies available for each species, the analyses of the qualitative data are descriptive and non-parametric.
The quantitative data were also grouped by genus for analysis, and null data or taxa with a prohibitively small number of records were excluded from the analyses, as necessary.Some hunting subcategories (medicinal use, pest control, and sports) were also excluded due to a reduced number of records.As the data were derived from field studies based on varying approaches and sampling effort, some adjustments were necessary to ensure reliable analyses.We used only the positive answers on hunting or trapping obtained in each study, for example, as a proportion of the number of informants interviewed.We analyzed the variation in the citations among the different primate genera by category (hunting or trapping) using Chi-square, and within each genus with the post hoc Bonferroni correction.We ran the analyses on the R platform v. 4.3.2(R Core Team 2023), using RStudio v. 2023.12.1.402(Posit team 2024), and the stats (R Core Team 2023) and chisq.posthoc.testpackages (Ebbert 2019), considering = 0.05 in all cases.

Qualitative Data
We identified 21 academic studies that contained 47 citations of species of all the six genera known to occur in the study area.These citations included four of Alouatta, two of Brachyteles, and three Leontopithecus, with eight for Callithrix, 14 for Sapajus, and 16 for Callicebus.Just over half of these citations (55.3%) referred to hunting and the other half (44.7%), to trapping (Figure 1; Additional File 1).In most cases (88.4%), the primates were hunted for bushmeat, although in all but one of the other records, the objective of the activity was not specified.Similarly, most (90.4%)citations of trapping referred to the capture of pets, while the remaining records were derived from scientific studies that involved trapping and trafficking surveillance.
All the citations of both Alouatta and Brachyteles referred to hunting for bushmeat (Table 1), while Leontopithecus was cited twice as game hunting and once for trapping pets.Predictably, based on its body size, Callithrix was targeted primarily as a source of pets (Table 1), and Sapajus was sought almost equally by hunters and trappers, whereas Callicebus was targeted mainly as game hunting.Titis (Callicebus), in turn, are notoriously difficult to maintain in captivity, in addition to their relatively small size (barely reaching one kilo), being a suboptimal target for subsistence hunters.One study (Jerusalinsky et al. 2013) indicated Callithrix as the most frequent genus as a pet, followed by Sapajus (Table 1).

Quantitative Data
Between 2006 and 2019, we surveyed 348 sites across the study area, and obtained 834 reports from local experts on the hunting and trapping of the local primate species.All these experts reported the local presence of Callithrix, while 818 cited Sapajus, and 738 referred to the genus Callicebus.Overall, 164 (30.4%) of the 539 informants questioned about the harvesting of bushmeat provided affirmative answer, while 189 (30.9%) of the 636 individuals consulted on the trapping of pets confirmed the practise.We recorded only one report of subsistence hunting for Alouatta caraya.As we did not interview all the informants comprehensively (see Methods), we selected 827 representative citations on subsistence hunting and 731 citations on trapping for analysis (Figure 2).Overall, Callicebus was cited most often as game (30.1%: 95 positive answers to 326 questions), while Sapajus was cited most often as a pet (35.7%: 80/224).Four informants reported hunting Sapajus for pest control because the capuchins damage their crops.
Overall (Figure 2), significant differences (χ 2 = 33.982;df = 2; p < 0.0001) were found among the three genera in the proportions of hunting and trapping.The post hoc analysis indicated that Callicebus was hunted significantly more frequently than it was trapped (p < 0.01), with the opposite pattern being observed in Sapajus (p < 0.01).However, while Callithrix was targeted more often for the capture of pets, the difference between the two types of exploitation was not significant (p = 0.607) in this case.

DISCUSSION
The historical data indicate that hunting and trapping are among the principal threats to primate populations, and that, after habitat loss and fragmentation, subsistence hunting is the principal driver of the local extinction of B. hypoxanthus, and the decline in the populations of howlers, A. caraya and A. guariba.These data also indicate that, while both Callicebus and Sapajus are targeted by hunters and trappers, Alouatta is target exclusively by hunters, and Callithrix for the acquisition of pets.The findings of the present study indicate clearly that hunting still threatens the populations of both Callicebus and Sapajus, although Alouatta is relatively rare or absent form most of the study area, which was reflected in the general paucity of reports, and may reflect habitat loss and hunting pressure.The absence of citations of Brachyteles was the result of local extinction in the areas surveyed.
In contrast with our expectations, Callicebus was one of the genera cited most often, both as game and pet, although this may reflect a sampling bias, given the number of the studies that focused specifically on this genus.As hunting is illegal in Brazil, it seems likely that the activity is largely under-reported, not only in monitoring programs (see Svensson et al. 2016), but also in specific research projects.The illegal nature of the activity will also likely reduce the presence of vestiges, that is, animal parts kept as tro-phies.While these questions almost certainly affected the findings of the present study, they were consistent with the historical data (i.e., Sapajus and Callithrix mostly trapped as pet; see details below).There is also the synergic effect of the capture of pets -orphaned infants -as a byproduct of hunting for bushmeat, which is not often dealt with adequately in the available studies.The detection of this synergic effect during fieldwork would be limited even more by the illegal nature of hunting.
Overall, in fact, there is a general lack of studies of the impact of hunting on most of the primate species found in the study area, although both Alouatta and Brachyteles have clearly been impacted extensively, as reported by Castilho et al. (2019) for A. guariba and B. hypoxanthus in southeastern Bahia.In addition to   2024) recorded low hunting rates in southern Bahia, which may nevertheless be the result of the few remnant populations that persist in the region.
While Alves et al. (2016) reported that Callicebus barbarabrownae was targeted only as a pet, Printes (unpub.data) recorded the medicinal use of this species, for the treatment of neurological disorder (for nerves' health, free transcription).According to Printes (pers.obs.), the informant reported eating only the flash (with no fat or organs) and did not describe any specific way of preparing.Worldwide, primates are hunted primarily for bushmeat, and secondarily for the pet trade, although traditional medicine and ornamental use are also minor factors in some cases (Ripple et al. 2016), but not in the present study.In some cultures, the hunting of primates is enhanced by local traditions (Bobo et al. 2015), whereas in other cultures, taboos limit the hunting and consumption of primates (Landim et al. 2023).As for other game mammal species (Alves et al. 2016(Alves et al. , 2023)), however, the hunting of primates for food tends to focus on medium-to large-body species (Ripple et al. 2016;Constantino 2018), as observed in the cases of Alouatta, Brachyteles, and Sapajus in the present study.Body mass is an important factor driving the decision making of hunters, who require an adequate tradeoff between effort and returns (Castilho et al. 2019).A secondary driver in the case of primate hunting is the taste of the meat.In Brazzaville, Congo, for instance, Mbete et al. (2011) identified that five species of Cercopithecus were preferred over 16 primate species.In the present study, however, the pet trade was the main secondary driver of primate hunting, so the value of pets should also figure in the equa-tion.The history of local human settlements may also be an important factor, given that primates are commonly used as pets (Parathian and Maldonado 2010) and are an important source of protein (Prado et al. 2012) among indigenous tribes.Thus, hunting could be a previous path for primate extinction in current settlements and villages in eastern Brazil, which may have been developed with the contribution of an earlier local indigenous culture.
Hunting inevitably leads to population decline (Silva et al. 2005(Silva et al. , 2016;;Canale et al. 2012;Madhusudan and Karanth 2002), although it can also have negative impacts on the behavior, vocalizations, and social structure of the hunted species (Thoisy et al. 2000;Papworth et al. 2013).In particular, the preference for females carrying young, which can be traded as pets (Silva et al. 2005) can have a major impact on social structure, and lead to a much more rapid decline in population numbers (e.g., Silva et al. 2016).
The impacts of hunting are determined by local biological, socioeconomic, and political contexts, which require complex conservation solutions (Barboza et al. 2016;Alves et al. 2023).In the present case, hunting has led to the local extinguished or drastic reduction in the populations of some species, which would require special attention in the planning of conservation strategies for the remaining populations.Protected areas play a crucial role in the protection and conservation of mammals, including game species and primates (Lee and Priston 2005;Canale et al. 2012), and the establishment of protected areas throughout the geographic range of the target species would be essential to prevent their extirpation.Despite the adequate federal legislation and the existence of a relatively well-structured monitoring system, it appears to be difficult to suppress hunting activities definitively in Brazil, and historically, most measures have been largely ineffective (Galetti and Dirzo 2013;Tomas et al. 2018;Alves et al. 2023).A potentially lucrative alternative would be to develop specific hunting agreements (Printes 2011;Oliveira and Calouro 2019) and management strategies (Alves et al. 2023;Almeida et al. 2023) aligned with the local characteristics of each biome, which could be tested in controlled trails to evaluate their effectiveness for the conservation of the target species.

ACKNOWLEDGMENT
We thank the Brazilian Coordination for the Improvement of Higher Education Personnel (CAPES) for the master (RB-M and EM) and doctoral (RB-M) fellowships during specific periods throughout the study period (Finance Code 001).We also thank the Brazilian National Council for Scientific and Technological Development (CNPq: processes 503372/2014-5 and 150123/2018-3) and the Brazilian Coordination for Higher Education Personnel Training (CAPES, process 88887.320996/2019-00)for the post-doctoral fellowships to RB-M.We are also grateful to CNPq (process 350639/2015-9) and the Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio: process SET-F 350639/2015-9) for the technical fellowship to ACA during the study period.RB-M was also supported by The Mohamed bin Zayed Species Conservation Fund (project no.162513903), Primate Action Fund (project no.1001257), and Primate Conservation Inc. (project no.1158).ACA was also supported by The Mohamed bin Zayed Species Conservation Fund (project no.162513903), and the Zoological Society for the Conservation of Species and Populations (ZGAP, facilitated through the NGO Pri-Matas).The field activities were partially funded by the Programa de Revitalização da Bacia Hidrográfica do Rio São Francisco of the Brazilian Ministry of the Environment and Fundação O Boticário de Proteção à Natureza (Project 0846_20092), as well as technical and operational support from the Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis (IBAMA/SE), Secretaria Estadual do Meio Ambiente e dos Recursos Hídricos de Sergipe (SEMARH/SE), and CODEVASF (Companhia de Desenvolvimento do Vale do São Francisco).We would like to express our gratitude to Gustavo Medeiros Netto (Morro de Pedra Farm), Antônio Estrela, Felipe Ferreira, and José Manoel Zelis Pereira for their invaluable support in the field.We would also thank Leandro Scoss and Míriam Plaza Pinto for their advice on the statistical analysis.

Figure 1 .
Figure 1.Relative frequency of reports of the hunting and trapping of the Neotropical primates of the states of Bahia and Sergipe, Northeastern Brazil, based on the academic literature published between 2005 and 2023.NI = Not Informed.

Table 1 .
Number of reports of the different uses of the Neotropical primate genera targeted by hunters in the Brazilian states of Bahia and Sergipe, based on the scientific literature published between 1997 and 2023.Genus Number of reports of game hunting for Bushmeat Pest control Not informed Capture of pets Scientific study Beltrão-Mendes et al. 2024.Hunting pressure on primates in the southern portion of the Brazilian Northeast: historical threats and current perspectives Ethnobiol Conserv 13:28

Figure 2 .
Figure 2. Relative frequency (percent) of citations of hunting and trapping of the three primate genera from the study area, based on interviews with 834 local residents at 348 sites distributed across the states of Bahia and Sergipe, in northeastern Brazil (data collected between 2006 and 2019).The asterisk (*) indicates a significant difference (p < 0.01) between the frequency of hunting and trapping in the respective genus.
Almeida et al. (2023), on the other, reported the game hunting of Callicebus coimbrai, in both mandatory reserves and privately-owned protected areas (RPPN -Reservas Particulares do Patrimônio Natural; Private Natural Heritage Reserves).Castilho et al. (2019) and Teixeira et al. (2024) recorded the game hunting of Callicebus melanochir in protected areas in southeast-ern Bahia, albeit at low frequencies.Callithrix is known to be hunted both for meat and the pet trade(Souza and Alves 2014;Barbosa et al. 2022;Alves et al. 2023), although(Alves et al. 2016) reported the medicinal use of these marmosets.In the present study region,Almeida et al. (2023) confirmed the widespread capture of Callithrix jacchus for pets, althoughCastilho et al. (2019) did not record any hunting of Callithrix kuhlii in southeastern Bahia.
Beltrão-Mendes et al. 2024.Hunting pressure on primates in the southern portion of the Brazilian Northeast: historical threats and current perspectives Ethnobiol Conserv 13:28 Callicebus coimbrai .The IUCN Red List of Threatened Species 2020:e.T39954A17972422.doi: 10.2305/IUCN.UK.2020-3.RLTS.T39954A17972422.en.Accessed on 16 March 2024.Beltrão-Mendes et al. 2024.Hunting pressure on primates in the southern portion of the Brazilian Northeast: historical threats and .ou to be continued... Beltrão-Mendes et al. 2024.Hunting pressure on primates in the southern portion of the Brazilian Northeast: historical threats and Beltrão-Mendes et al. 2024.Hunting pressure on primates in the southern portion of the Brazilian Northeast: historical threats and current perspectives