Introduction
Traditional knowledge is a cumulative body of expertise, awareness and beliefs, culturally transmitted across generations, concerning the relationships of living beings among themselves and with their environment (Berkes et al., Reference Berkes, Colding and Folke2000). Originating from daily interactions with the environment (Fabricius & Koch, Reference Fabricius and Koch2004), it underpins an understanding of ecosystem processes at temporal and spatial scales that would be difficult to record by conventional scientific research (Huntington, Reference Huntington2000). Traditional knowledge can therefore guide efforts towards the protection of habitats, supporting conservation actions at the species level (Huntington, Reference Huntington2000; Rajamani, Reference Rajamani2013).
The Amazonian manatee Trichechus inunguis has been the most hunted aquatic mammal in Brazil since pre-colonial times (da Silva et al., Reference da Silva, Rosas, Cantanhede, Machado, Drummond and Paglia2008) and consequently has suffered significant decline. It is categorized as Vulnerable on the national list of threatened species and the IUCN Red List (MMA, 2014; Marmontel et al., Reference Marmontel, de Souza and Kendall2016), and is listed in Appendix I of CITES (CITES, 2017). Despite a decrease in hunting (Marmontel et al., Reference Marmontel, Rosas, Kendall, Hines, Reynolds, Aragones, Mignucci-Giannoni and Marmontel2012), the consumption of manatee meat is still customary in the Amazon (ICMBio, Reference Andrade, Luna and Reis2011).
This aquatic mammal lives its entire life in the water, reaches up to 3 m in length and 420 kg (Amaral et al., Reference Amaral, da Silva and Rosas2010), and is herbivorous, feeding on macrophytes, roots and vegetation from floodplains (Best, Reference Best and Sioli1984; Guterres-Pazin et al., Reference Guterres-Pazin, Marmontel, Rosas, Pazin and Venticinque2014) with distinct physical and chemical properties, such as black and clearwater, flooded forests (igapós), and whitewater rivers (várzeas; Best, Reference Best1983; Rosas, Reference Rosas1994). The differences between these environments are paralleled in the variations in richness and diversity of plants the manatee feeds upon (Crema, Reference Crema2017).
Studying the Amazonian manatee is challenging because of its cryptic behaviour, the turbidity of its favoured habitats (Best, Reference Best and Sioli1984; Rosas, Reference Rosas1994) and its ability to spend long periods beneath banks of aquatic macrophytes (Junk & da Silva, Reference Junk, da Silva and Junk1997). However, people living in riverine communities have been able to share detailed knowledge about this species because historically they have shared and used the same environment (Calvimontes & Marmontel, Reference Calvimontes, Marmontel, Fuentes, Silva, Méndez, Azúa, Mejí and Santillan2010).
We sought to elicit traditional knowledge about T. inunguis (places of occurrence, reproductive season, diet, hunting, cultural importance) in federal protected areas in black and clearwater igapós in the Brazilian Amazon, to answer the following questions: (1) Are the diet of T. inunguis and the floristic composition of its habitat determined by the characteristics of each specific igapó? (2) Can traditional knowledge improve our scientific knowledge of the biology and conservation of the Amazonian manatee?
Study areas
The study was conducted in two regions: (1) Anavilhanas National Park, including residents of the municipality of Novo Airão and 14 communities of three protected areas in Amazonas State (the Environmental Protection Area on the right bank of the Rio Negro Paduari–Solimões Sector, the North Sector of Rio Negro State Park, and the Environmental Protection Area on the left bank of the Rio Negro Aturiá–Apuauzinho Sector); (2) the Tapajós region, where residents from six communities of the Tapajós–Arapiuns Extractive Reserve and three communities of the Tapajós National Forest were interviewed.
Anavilhanas (647,610 ha) is an area of integral protection in the municipality of Novo Airão, 60 km from Manaus (ICMBio, 2017). It was established as an Ecological Station in 1981 and designated a National Park in 2008. The majority of its area comprises seasonally flooded, fluvial islands, and the remainder is unflooded terra firme forest. The Tapajós National Forest (600,000 ha) was established in 1974 in the municipalities of Aveiro, Belterra, Rurópolis and Placas, Pará State (IBAMA, 2004). The Tapajós–Arapiuns Extractive Reserve (647,610 ha) was created in 1998 in the municipalities of Santarém and Aveiro, Pará State (ICMBio, 2014). In Tapajós National Forest and Tapajós–Arapiuns Extractive Reserve, separated by the Rio Tapajós, sustainable use of natural resources is permitted; both banks of the Rio Tapajós are largely covered by terra firme forest, with ria lakes and thin strips of igapó forest.
Methods
We selected interviewees from among the caboclos, the riverine people whose ancestry is a mix of Indigenous, Afro-Brazilian and European peoples (Lima-Ayres, Reference Lima-Ayres1992). Interviewees were selected according to three criteria: (1) experience in hunting manatees, or any direct contact with the species, (2) at least 19 years living in the area, and (3) the recommendation of community leaders. Interviews were conducted between March 2012 and October 2014, with 29 men and one woman in Anavilhanas, 34 men and four women in Tapajós–Arapiuns Extractive Reserve, and 19 men and three women in Tapajós National Forest (90 participants in total).
The interviews were semi-structured (Supplementary Material 1) and included questions about the occurrence and biology of the Amazonian manatee, focusing in particular on its feeding ecology. Part of the interview consisted of a free-listing activity (Borgatti, Reference Borgatti, Schensul and Le Compte1998; Albuquerque et al., Reference Albuquerque, Ramos, Lucena, Alencar, Albuquerque, Cunha, Lucena and Alves2014) in which the interviewees listed plants eaten by the manatee (Best, Reference Best1981; Colares & Colares, Reference Colares and Colares2002; Franzini et al., Reference Franzini, Castelblanco-Martinez, Rosas and da Silva2013; Guterres-Pazin et al., Reference Guterres-Pazin, Marmontel, Rosas, Pazin and Venticinque2014). A board with 39 photographs of plant species of the region was shown, and interviewees were asked to name the plants. Maps were created based on observations by the interviewees of manatees and signs of manatee occurrence (faeces, feeding traces, mortality).
In addition, we identified the locations of comidias (feeding areas), which are open areas in the aquatic vegetation resulting from the feeding of manatees (Calvimontes & Marmontel, Reference Calvimontes, Marmontel, Fuentes, Silva, Méndez, Azúa, Mejí and Santillan2010). Aquatic macrophyte vegetation was surveyed using line transects along the vegetated margins of lakes, as described by Crema (Reference Crema2017). In Anavilhanas 43 sites of occurrence were identified, five of them outside the protected area (Fig. 1a); 30 sites were recorded in the Tapajós region (Fig. 1b). We grouped plant species based on life-form (adapted from Junk, Reference Junk, Davies and Walker1986), following the nomenclature of Forzza et al. (Reference Forzza, Costa, Walter, Pirani, Morim and Queiroz2016). Plant species identified from the 73 sites were deposited in the herbarium at the Federal University of Amazonas (HUAM, Manaus, Brazil).
Fig. 1 Locations of sightings and evidence of feeding of the Amazonian manatee Trichechus inunguis in (a) Anavilhanas National Park and (b) protected areas in the Tapajós region.
The data from the listing of plant species by interviewees were used to calculate a cognitive salience index (Sutrop, Reference Sutrop2001). This index (S) represents the summed importance of each plant, combining the frequency of citation of an item (F) in interviews with its mean position on all lists (mP): S = F/(N × mP), where N is the total number of the plant species named during the interviews.
Results
Interviewees were aged 32–83 years in Anavilhanas and 19–82 in the Tapajós region. None of the respondents claimed to be engaged in manatee hunting activity at the time of the interviews, but four indicated they had hunted when they were younger. Twenty per cent of the interviewees reported having seen manatees in the previous 2 years in Anavilhanas, and 56% in the Tapajós region (Table 1). The number of manatees reported killed by hunting in the previous 10 years was much higher in Anavilhanas (30% of the interviewees) than in Tapajós (5%; Table 1); the high-water season was considered to be the best time to see manatees (59% in Anavilhanas; 80% in Tapajós; Table 1).
Table 1 Principal responses to questions, provided by riverine people in Anavilhanas National Park (Fig. 1a) and protected areas in the Tapajós region (Tapajós National Forest and Tapajós–Arapiuns Extractive Reserve; Fig. 1b) in interviews (Supplementary material 1) about the Amazonian manatee Trichechus inunguis, with the number and percentage of interviewees who gave each response.
Most interviewees (72% in Anavilhanas and 32% in Tapajós) stated that manatees move in pairs, often a female with a calf. In Tapajós 40% had seen groups of up to four individuals; in Anavilhanas larger groups had been seen (33%; Table 1). In Anavilhanas and Tapajós 68% and 95% of interviewees, respectively, stated that during the low-water season the species migrates to deeper water areas (poços) and to the riverbeds. In Anavilhanas 81% of interviewees indicated they had not observed manatee sexual activity, whereas in Tapajós 60% said that this occurs during the flooding season (Table 1).
Feeding habits
Interviewees indicated that 60 plant species are consumed by the Amazonian manatee, 31 in Anavilhanas and 37 in Tapajós, with 12 species common to both areas (Table 2). Seventeen of the plant species (mainly vines) cited by interviewees were not in the photographs shown, but the interviewees described the plants in detail and we were able to collect them. In Anavilhanas the plant species with the highest cognitive salience index values were the vines Ipomoea alba, Mikania micrantha, Tassadia berteriana and Mesechites trifida, followed by the shrub Coccoloba pichuna (Table 3). In Tapajós the plant species with the highest cognitive salience index values were herbaceous plants with floating leaves such as Nymphaea spp., and rooted submerged plants such as Eleocharis minima and Eleocharis fluctuans (Table 3). In Tapajós 70% of the respondents indicated that manatees also feed on submerged plant roots, mainly of Nymphaea spp.
Table 2 List of plant species in the diet of the Amazonian manatee, as reported during interviews with riverine people in Anavilhanas National Park (A) and protected areas in the Tapajós region (T), complemented with reports from the literature.
1Franzini et al. (Reference Franzini, Castelblanco-Martinez, Rosas and da Silva2013).
2Guterres-Pazin et al. (Reference Guterres-Pazin, Marmontel, Rosas, Pazin and Venticinque2014).
3Best (Reference Best1981).
4Colares & Colares (Reference Colares and Colares2002).
5Best & Teixeira (Reference Best and Teixeira1982).
Table 3 Citation frequency, mean citation position on all lists, and cognitive salience index value of each plant species reported by interviewees from the vicinity of Anavilhanas National Park, and the Tapajós National Forest and Tapajós–Arapiuns Extractive Reserve as being a component of the diet of the Amazonian manatee, ordered by descending cognitive salience index. Only those species from Table 2 that were cited in more than one interview are listed here.
Hunting
Hunting was reported by interviewees to be the main cause of death of the species (62% of interviewees in Anavilhanas and 52% in Tapajós), but in Tapajós 16% of interviewees also reported that manatees died from stranding and entanglement in fishing nets (Table 1). Most hunting records predate 2003 (42 and 75% in Anavilhanas and Tapajós, respectively; Table 1). In Anavilhanas 26% of respondents were aware of hunting events, compared to 2% in Tapajós. The harpoon was the most cited hunting instrument, and high-water season the hydrological phase with the highest hunting intensity (68 and 90% in Anavilhanas and Tapajós, respectively), although 23% of respondents in Anavilhanas said that hunting occurs throughout the year (Table 1). The most cited motivation for hunting was subsistence, but trade was also mentioned (22% of all interviewees). A majority of all interviewees (65%) admitted to having consumed manatee meat (Table 1), at least in their youth, and some interviewees from Anavilhanas said they knew of small markets where manatee meat was sold. Most claimed that manatee fat can be used in cooking (77 and 91% in Anavilhanas and Tapajós, respectively), and medicinal use was cited frequently in Tapajós (32%; Table 1).
Discussion
The traditional knowledge of the riverine people interviewed corroborated the findings of other researchers (Best, Reference Best and Sioli1984; Arraut et al., Reference Arraut, Marmontel, Mantovani, Novo, Macdonald and Kenward2010) and highlighted the influence of seasonal ecosystem changes on the distribution of Amazonian manatees:
During high-water periods, they eat in the shallow places, at night.
In the summer (low-water season) we cannot find it, there is no food, nothing. They only surface in deep areas.
Although the interviewees’ level of knowledge of manatee reproduction varied, some described the reproductive behaviour of a female, with several males, as described by Pereira (Reference Pereira1944). Several interviewees reported the birth of calves, confirming the observations of Best (Reference Best1982): it occurs as waters rise, when there is greater availability of plants. In agreement with Rosas (Reference Rosas1994), interviewees reported that manatees were usually solitary or with calves. However, they also described having seen large groups of manatees, especially in low-water seasons, in refuges. Other types of aggregations have been reported at feeding sites (Best, Reference Best1982) and during the reproductive period (Pereira, Reference Pereira1944; Souza, Reference Souza2015).
Feeding habits
From the interviews and the collection of plants both in Anavilhanas and the Tapajós region (Crema, Reference Crema2017), 60 food species were recorded, of which 40 (67%) had not previously been known to be food plants (Best, Reference Best1981; Colares & Colares, Reference Colares and Colares2002; Zaniolo, Reference Zaniolo2006; Franzini et al., Reference Franzini, Castelblanco-Martinez, Rosas and da Silva2013; Guterres-Pazin et al., Reference Guterres-Pazin, Marmontel, Rosas, Pazin and Venticinque2014), indicating there is a significant amount of traditional knowledge yet to be gathered on the feeding ecology of wild Amazonian manatees. In contrast with findings that plants of the families Cyperaceae and Poaceae are the most important food plants for the Amazonian manatee (Best, Reference Best1981; Colares & Colares, Reference Colares and Colares2002; Guterres-Pazin et al., Reference Guterres-Pazin, Marmontel, Rosas, Pazin and Venticinque2014), in Anavilhanas the cognitive salience index indicated that a number of other species are important, including vines and shrubs. These become accessible to manatees during the high-water season, when shrubs are flooded and the lower leaves of vines become accessible (Crema, Reference Crema2017).
In Anavilhanas there is no evidence of plant consumption by manatees during the low-water season. However, a study in central Amazonian igapós identified a variety of species in the faeces and stomach contents of manatees in this season (Guterres-Pazin et al., Reference Guterres-Pazin, Marmontel, Rosas, Pazin and Venticinque2014). Anavilhanas does not have significant availability of food for aquatic herbivores during most of the year (Crema, Reference Crema2017). In the low-water season some plant species predominate only in permanently wet places, inaccessible to the manatee. During high waters, when food is more available, manatees accumulate fat to survive the dry season (Best, Reference Best1983). Thus, the manatee exhibits selective or opportunistic feeding behaviour, depending on the availability of plants, which is related to the flood pulse (Colares & Colares, Reference Colares and Colares2002; Guterres-Pazin et al., Reference Guterres-Pazin, Marmontel, Rosas, Pazin and Venticinque2014). According to the traditional knowledge of riverine people, in the Tapajós region the manatee selects rooted plants with floating leaves and, although it feeds preferentially on leaves, it may also dig up the lake bed around Nymphaea spp. to consume their corms and roots. In Tapajós many lakes retain sufficient water during the low-water season to support the persistence of both submerged macrophytes and manatees (Crema, Reference Crema2017).
Hunting
As already reported (Pereira, Reference Pereira1944; Marmontel et al., Reference Marmontel, Rosas, Kendall, Hines, Reynolds, Aragones, Mignucci-Giannoni and Marmontel2012), manatee hunters have specific knowledge about the species. At both study sites comidias are an indicator for locating manatees during the high-water season. Hunting of the Amazonian manatee is related to its variation in habitat use (Calvimontes & Marmontel, Reference Calvimontes, Marmontel, Fuentes, Silva, Méndez, Azúa, Mejí and Santillan2010; Souza, Reference Souza2015). Some authors (Best, Reference Best1982; Calvimontes & Marmontel, Reference Calvimontes, Marmontel, Fuentes, Silva, Méndez, Azúa, Mejí and Santillan2010), and the interviewees in our study, reported that during low water hunting is restricted to pools where several manatees congregate and members of the community fish, increasing the potential for encounters between them (Mayaka et al., Reference Mayaka, Awah and Ajonina2013).
As cited for other localities (Marmontel et al., Reference Marmontel, Rosas, Kendall, Hines, Reynolds, Aragones, Mignucci-Giannoni and Marmontel2012), interviewees confirmed that harpoon hunting is the primary cause of death of Amazonian manatees, followed by incidental catches in fishing nets (Aguilar, Reference Aguilar2007; Zaniolo, Reference Zaniolo2006), particularly of vulnerable young individuals. Such impacts can substantially reduce populations (Rosas, Reference Rosas1994).
In 1938 peak demand for T. inunguis hide led to the hunting of c. 16,000 manatees (Domning, Reference Domning1982; Antunes et al., Reference Antunes, Fewster, Venticinque, Peres, Levi, Rohe and Shepard2016). Since the creation of the Fauna Protection Act in 1967 there has been no record of this type of activity. Therefore, the motivation for hunting is small-scale commercialization and an appreciation, or tradition, of manatee meat consumption (Calvimontes & Marmontel, Reference Calvimontes, Marmontel, Fuentes, Silva, Méndez, Azúa, Mejí and Santillan2010; da Silva et al., Reference da Silva, Shepard, do Carmo, Guillaume and Velden2017).
The use of protected areas by Amazonian manatees
The locations shown in Fig. 1 indicate places of rest, refuge or foraging for the Amazonian manatee, information fundamental for defining sites for release and management of the species. Releases of rehabilitated manatees to recolonize Amazonian water bodies were carried out in 2007 in Tapajós–Arapiuns Extractive Reserve, during 2008–2009 in Rio Cuieiras (Rio Negro Basin), in 2012 in Amanã Reserve, and in 2016–2018 in Piagaçu–Purus Reserve (Diogo Souza, pers. comm.). Knowledge of places with suitable foraging resources can provide alternative locations for the release of manatees.
Although the studied areas are protected by law, in Anavilhanas 30% of the respondents reported at least one episode of manatee hunting during the 2 years preceding our research. Anavilhanas has a small human population, historically characterized by inter-ethnic conflicts, loss of cultural identity, and economic hardship that made exploitation of natural resources essential for survival (Leonardi, Reference Leonardi1999). The Park receives a large number of visitors, and its proximity to urban centres increases its vulnerability to anthropogenic disturbances (Tardio & da Silveira, Reference Tardio and da Silveira2015) and illegal activities (ICMBio, 2017).
The number of hunting events recorded in recent years is fewer in Tapajós, which may be attributed to fear of reporting illegal events, or a reduction in hunting practices, strengthened by traditional knowledge. The Tapajós region comprises sustainable use areas, where rational and sustainable exploitation is permitted. The creation of the Tapajós–Arapiuns Extractive Reserve was driven by a popular movement (IBAMA, 2004; ICMBio, 2014) and the inhabitants are considered to be traditional, having a history of multi-generational residence and sustainable use of natural resources (Berkes et al., Reference Berkes, Colding and Folke2000).
In Anavilhanas traditional knowledge highlighted the importance of vines as a component of manatee diet, despite being available only during the high-water season. As in this region there is little or no food available for aquatic herbivores during flooding (Crema, Reference Crema2017), manatees may move to areas with higher food supply, such as the Rio Solimões floodplain, c. 130 km away, which is rich in aquatic plants (Piedade et al., Reference Piedade, Ferreira and Franco2010). The Amazonian manatee performs annual migrations of tens of kilometres between ecosystems (Arraut et al., Reference Arraut, Marmontel, Mantovani, Novo, Macdonald and Kenward2010). Thus, conservation initiatives for T. inunguis in Anavilhanas need to be broadened to a larger area to ensure its protection.
Elsewhere, environmental conservation has been found to be related to education level (Fiallo & Jacobson, Reference Fiallo and Jacobson1995). Through involving fishers in ecotourism and research, the Mamirauá Institute of Sustainable Development and Projeto Boto have promoted positive attitudes towards the conservation of the Amazon river dolphin Inia geoffrensis (Mintzer et al., Reference Mintzer, Schmink, Lorenzen, Thomas, Martin and da Silva2015). We have discussed the nature of effective manatee conservation with protected area authorities, emphasizing that a suitable strategy must not only limit hunting but also increase the involvement of riverine people in management activities. Studies are also required to determine the range of the manatee, so that joint actions between all protected area stakeholders can be planned. Combining the management of these areas with the active participation of the local population is one of the greatest challenges and opportunities for conservation (Fragoso et al., Reference Fragoso, Silvius and Villa-Lobos2000; Shepard et al., Reference Shepard, Rummenhoeller, Ohl-Schacherer and Yu2010).
The diet of the Amazonian manatee differs between igapós because of differences in the floristic characteristics of each. Riverine people in the vicinity of Anavilhanas and Tapajós protected areas have detailed knowledge of the biology of the Amazonian manatee and of plant species that had not been previously reported to be part of the manatee's diet. Improving social participation, including this important knowledge, is fundamental for the conservation management of the Amazonian manatee and its habitat.
Acknowledgements
We thank Eliene Cruz and Graziela Balassa for the map figures, the HUAM and all those who have helped with this study. Financial support was provided by Instituto Chico Mendes de Conservação da Biodiversidade, Grupo Ecologia Monitoramento e Uso Sustentável de Áreas Úmidas; Adaptações da Biota Aquática Amazônica II, Associação Amigos do Peixe-boi, and Projeto Petrobras Socioambiental. Field work was carried out under collecting permits CEUC/SDS 70/2014 and SISBIO 25347/2011, provided by Centro Estadual de Unidades de Conservação of Amazonas State and Instituto Chico Mendes de Conservação da Biodiversidade, respectively.
Author contributions
Project design: LCC, VMFS and MTFP; data collection and writing: LCC; data interpretation and revision of the text: all authors.
Conflicts of interest
None.
Ethical standards
Research was approved by the Human Research Ethics Committee of the National Institute of Amazonian Research (#501,473/2013) and followed national laws.
