Research

INTRODUCTION

Forest management is the implementation of sustainable practices that maintain forest changes and extend environmental, economic, or sociocultural conservation objectives (FAO 2022). Indigenous perspectives on forest management are grounded in traditional ecological knowledge (TEK), a transformative and cumulative body of knowledge-practice-belief about the relationships of living beings (including humans) with one another and with their environment (Berkes et al. 2000). Sociocultural elements associated with TEK (e.g., cosmologies, social relations, species knowledge, etc.) influence Indigenous forest management (Poffenberger and McGean 1993, de Oliveira 2016), which, in turn, influence forest successional processes (Gómez-Pompa 1987, Balée and Gély 1989, Douterlungne et al. 2010). However, how such sociocultural elements structure Indigenous perspectives on forest management is unclear. Moreover, little is known about how Indigenous management influences forest succession and floristic diversity. Understanding these issues is paramount, because Indigenous TEK represents a source of new social-ecological concepts, conjectures, and theories that can improve our ability to understand and sustainably act on social-ecological systems (Tengö et al. 2014, Coscieme et al. 2020).

Social-ecological systems represent the interconnection between biological and cultural diversities, which is called biocultural diversity (Gavin et al. 2015, Hill et al. 2019). Studies on biocultural diversity have suggested that social-ecological systems are structured by keystone biocultural traits (i.e., social-ecological relationships with specific taxa), whose top-down effects on biocultural diversity are large relative to other elements within the systems (Winter et al. 2018). These keystone biocultural traits promote effects in ecological processes and patterns (Franco-Moraes et al. 2021), generate biocultural unities (i.e., relationships shared by the same group of people) for social-ecological systems (Reyes-Valdés and Kantartzi 2020), and influence management sustainability (Datta 2015). In social-ecological systems that are dependent on shifting cultivation, an important indicator of sustainability is the resilience of forest regrowth in fallows (Lawrence et al. 2010). The main factor limiting resilience in forest recovery is land-use intensification (Jakovac et al. 2015), and the most common proxy used for assessing forest recovery is basal area increment (Nikinmaa et al. 2020). Therefore, it is expected that key social-ecological relationships structure the ways Indigenous Peoples understand forest management, thus influencing resilience as measured by the basal area increment during forest regrowth in fallows.

Amazonia has some of the richest biocultural diversity in the world (Loh and Harmon 2005). Amazonian Indigenous Peoples understand that non-humans (i.e., animals, plants, etc.) involved in social-ecological relationships have social lives (de Castro 1998, Descola 2005) and transform landscapes according to their own interests (da Cunha 2019). For sociocultural reasons associated with social-ecological relationships, these peoples value and promote the presence of different non-humans and the existence of different landscapes (da Cunha 2017, Fausto and Neves 2018, Fausto 2019). For example, Amazonian Indigenous TEK values swiddens containing different species and species varieties (Emperaire 2005, Rival and McKey 2008, da Cunha 2017). This appreciation leads these peoples to promote inter- and intra-specific differences in their swiddens (Perrault-Archambault and Coomes 2008, de Oliveira 2019, Emperaire et al. 2021).

When Indigenous swiddens are harvested they give way to fallows where forest regrowth can occur sustainably, often in association with management of remnant crops and trees/palms (Levis et al. 2018, Franco-Moraes et al. 2019). Although Indigenous understandings of sustainability vary (Fernández-Llamazares and Virtanen 2020, Virtanen et al. 2020), TEK of most Amazonian Indigenous Peoples considers that forest sustainability requires opening and fallowing of swiddens in space-time, i.e., shifting cultivation (Denevan 2001). This practice prevents land-use intensification and engenders different forest successional stages at the landscape-level (Saldarriaga et al. 1988, Franco-Moraes 2021). Because these stages contain different species and represent distinct landscapes (Finegan 1996, Chazdon 2003, Mesquita et al. 2015), it is expected that Amazonian Indigenous TEK values not only different swiddens, but also different forest successional stages, so that local perspectives on forest management are based on social-ecological relationships associated with such understanding.

In many Indigenous Amazonian social-ecological systems, relationships with non-humans occur through an ethic of moderation, i.e., through behaviors of decorum and precaution (Lévi-Strauss 1968, Gallois 1988, Aparício 2020). Among the Zoʻé, an Indigenous People of recent contact in northern Brazilian Amazonia, these behaviors include not overhunting diverse types of game (or during inappropriate periods), and moving away from game in some situations because they can be vindictive, which causes a necessary social distancing in relation to game (Braga et al. 2020). This distancing influences Zoʻé mobility, because the practice of opening and fallowing swiddens in new regions results, among other reasons, from this ethic of moderation in relation to game (Havt 2001, Braga 2021a). This practice, in turn, should lead to higher alpha diversity (i.e., at the local level) in old swidden-fallow patches with an intermediate successional recovery time (counting since the last disturbance), because these patches encompass both opportunistic and competing species (Sheil and Burslem 2013).

Higher biodiversity in forests with intermediate levels of disturbance, whether in relation to frequency, intensity, or the time elapsed since it occurred, is a classical hypothesis in ecology known as the intermediate disturbance hypothesis (IDH; Connell 1978). Although implications of the IDH are debatable, and some attempts to corroborate them failed (Fox 2013, Barabás et al. 2018), empirical support for IDH in tropical forest plant communities is increasingly reported (e.g., in relation to disturbance intensity and frequency; Molino and Sabatier 2001, Svensson et al. 2012, Guitet et al. 2018). In fact, the IDH represents a general framework that can regroup various hypotheses regarding specific disturbance mechanisms and the level of biodiversity across space and time (Sheil and Burslem 2013). From the IDH framework, we can also expect that Zoʻé shifting cultivation should lead to higher beta diversity (i.e., at the landscape level) by creating forest patches with different alpha-diversities and compositions (Balée 2006, Guèze et al. 2015, Odonne et al. 2019).

Shifting cultivation has been a widespread practice among Amazonian Indigenous Peoples for thousands of years (Denevan 2001). Although some authors have shown that intensification of shifting cultivation reduces recovery of floristic diversity and structure (Jakovac et al. 2015, Villa et al. 2018), others have shown that recovery can occur over time (Saldarriaga et al. 1988, Mukul et al. 2020). Testing the IDH for forest recovery time in Indigenous social-ecological systems can help us understand the long-term consequences of shifting cultivation (Balée 2006), thus contributing useful information to environmental agendas aimed at the resilience of social-ecological systems (Sterk et al. 2017). For this, sociocultural aspects should be considered, because they influence the way Indigenous Peoples transform their landscapes (Franco-Moraes et al. 2021). Cosmological aspects, for example, are behind Indigenous Peoples’ management practices and are critical for ensuring long-term sustainability of Indigenous social-ecological systems (Fernández-Llamazares and Virtanen 2020).

We present a case study among the Zoʻé that aims to determine if there is a key social-ecological relationship that structures the Zoʻé’s perspective on forest management. We collected ethnographic information about Zoʻé TEK on forest succession, and about behaviors of decorum and precaution. We also investigated if such a relationship guided management that generated resilient forest regrowth along a gradient of forest patches in different successional stages that encompass old swidden-fallow areas and old-growth forests. For this, we compared forest structure (basal area and ethnospecies density) along the gradient. Finally, we tested (1) if alpha diversity is maximal in forest patches of intermediate age, i.e., patches that have been regenerating for decades but have not reached their mature state, and (2) if the gradient of forest patches promoted beta diversity at the landscape scale. For this, we assessed ethnospecies richness and diversity (alpha diversity), and ethnospecies relative abundance and floristic composition (beta diversity) along the gradient.

METHODS

Study area and population

Fieldwork was conducted on the Zoʻé Indigenous land (Fig. 1a). Local landscapes are composed of large, open terra-firme forest areas, várzea forest areas, and small-medium patches of savannah (Pires and Prance 1985). Soils are similar among forested areas: they are acidic, nutrient-poor, have a low cation-exchange capacity, and are predominantly red-yellow Podzols and Oxisols (Venturieri et al. 2000). The climate is seasonal, humid tropical with a rainy season between December to June and a dry season between July to November. Mean annual rainfall and temperature are 2192 mm and 27.5 °C, respectively (INMET 2020).

The Zoʻé are a people of recent contact that live on their Indigenous land, which was ratified in 2009, and is located in interfluvial forests between the Cuminapanema and Erepecuru Rivers, in northern Pará State, Brazil. They were officially contacted in 1982 by missionaries of the New Tribes Mission, who started living near Zoʻé villages to evangelize them. In 1991, after a fifth of the Zoʻé population had died of diseases transmitted by non-Indigenous People, the National Indian Foundation (FUNAI) removed the missionaries and created a base in the region (Iepé and FPEC 2019).

Currently, 320 Zoʻé live on their Indigenous land. They speak a language of the Tupi-Guarani family, and some local chiefs and young people also speak Portuguese; hereafter, terms in the Zoʻé language appear in italics. The Zoʻé are divided into four local groups that alternate periods in semi-permanent villages and in temporary camps, and their management system consists of shifting cultivation, hunting-gathering, and fishing (Iepé and FPEC 2019).

Data collection

Ethnographic data

Ethnographic data, including semi-structured and structured interviews, were collected during a 45-day expedition (May–June 2019) that we carried out together with members of different Zoʻé families (Fig. 1b); the expedition occurred as part of seasonal hunting-gathering activities carried out by the Zoʻé. Semi-structured interviews based on directed but open-ended questions offered greater flexibility to probe oral histories and other aspects of TEK (Bernard 1988). Semi-structured interviews about historical occupation, mobility, and management practices were conducted with 12 men aged 26 to 74. Structured interviews, which were appropriate for obtaining responses to ordered questions (Bernard 1988), involved describing the usefulness of the most abundant ethnospecies present in our plots and were conducted with five men aged 36 to 74 and one woman aged 54. We also collected information about cosmology, social relations, mobility, and occupation history among the Zoʻé from the available literature (Braga 2017, 2021a, Braga et al. 2020, Gallois et al. 2020).

Floristic data

During our expedition, we stayed for a few days in four regions pre-established by the Zoʻé according to their travel plan. In these regions, we carried out floristic inventories in fallowed forest patches that were left in succession from nine to ~140 years ago (Fig. 1c; Table 1), counting from the last clearance until 2019 (although the Zoʻé returned to them to open temporary camps). The year the area was left in succession was calculated from documents and/or Zoʻé ancestral memory (Appendix 1). This sampling method (called chronosequence), allowed us to view temporal products of successional dynamics by analyzing floristic patterns of different forest successional stages (Walker et al. 2010). Overall, our sampling encompassed forest patches with ages varying from 9, 17, 28, ~70 to ~140. In three of the four regions, we carried out an inventory in a forest patch where the Zoʻé said they had never cleared, although they had hunted and collected there. Because of logistical issues, this type of forest was not sampled in the southernmost region and could only be sampled once in each of the other three regions. These forest patches were the closest representation we could find of old-growth forests, which are defined as forests in a late stage of succession that were not subjected to large disturbances in the past, such as clearance for swiddens (Chazdon 2014). In 2019, the Zoʻé had an ancestral memory of eight generations (Appendix 1), so we inferred that these three old-growth forests had not been cleared for at least 140 years (Table 1).

Forest patches in which plots were established were selected considering oral histories, logistical issues, and the availability of Zoʻé collaborators. To avoid floristic differences associated with soil variability in our samples, we only carried out inventories in patches with black soil (ywy byk, which, according to Zoʻé, are soils suitable for swidden; archaeological surveys are being done to verify if ywy byk represents Amazonian Dark Earth). In addition, because the vast majority of tree and palm species in tropical forests disperse seeds less than 100 m (Kettle 2012), to avoid short-distance seed dispersal effects among plots within the same region we established plots at distances greater than 100 m (Table 2). Nevertheless, long-distance seed dispersal by mammals and birds can influence floristic variability, mainly within a radius of 1.5 km (Link and Di Fiore 2006, Kitamura 2011). Soil collection was not authorized by the Zoʻé.

Because Zoʻé swiddens are ~0.5 ha (JF-M, personal observations), to capture floristic variability across the forest patch (Gordon and Newton 2006), we established four subplots of 25 x 10 m (0.025 ha) for floristic inventories in each forest patch, so that the sum of these subplots corresponds to one plot of 0.1 ha. With randomized sampling, we established two subplots in different edges and two subplots in different areas of the center of the patches. For basal area assessments, we measured the CBH (circumference at breast height) of all trees/palms ≥ 10 cm, i.e., 3.18 cm DBH (diameter at breast height). This is an appropriate threshold as reliable basal area assessments for plot sizes of 0.1 ha in Amazonia should include DBH thresholds < 10 cm (Oliveira et al. 2014).

Ethnospecies identification

Because we were interested in Zoʻé TEK on floristic composition, all trees/palms ≥ 10 cm CBH were identified with Zoʻé ethnospecies names. A Zoʻé specialist of trees/palms identification, (Biri, a 74-year-old Zoʻé man who in 2019 owned land in areas we visited and who best knew the regions) accompanied us throughout data collection, along with another 19 Zoʻé collaborators, all of whom participated in identification. Ethnospecies identification by the Zoʻé was based on their own morphological, phenological, and social-ecological criteria, so that these ethnospecies might not necessarily match scientific taxa. Although we understand the importance of scientific identification for these ethnospecies for purposes of comparisons with other studies, plant collection was not authorized by the Zoʻé. However, because some ethnospecies were also identified by popular names by the Zoʻé, in a few cases we were able to identify them with a scientific name, because such popular names were scientifically well established; in the text, such ethnospecies are presented with their respective scientific names. We also investigated the local use of the most abundant trees/palms by grouping them into five categories: food, manufacturing, therapeutic, construction, and fuel (Prance et al. 1987, Phillips and Gentry 1993).

Floristic data analysis

To investigate differences among plots, we compared alpha- and beta diversity, composition, and structure. As a proxy for alpha-diversity (intra-plot diversity), we calculated the ethnospecies richness for each plot using a species rarefaction curve (Gotelli and Colwell 2001). As a proxy for beta diversity (inter-plot diversity), we compared dissimilarity among plots in relation to the relative abundance of the 10 most abundant ethnospecies in each plot, totaling 47 ethnospecies (~70% of the total abundance of all plots). We used non-metric multidimensional scaling (NMDS) with ordination in one dimension (McCune and Grace 2002) and applied the Bray-Curtis dissimilarity index (Faith et al. 1987). Although this analysis does not represent a statistical hypothesis test, by sorting plots along a gradient of relative abundance, it showed possible floristic variability among plots, which is beta diversity (Whittaker 1967, Faith et al. 1987). To compare diversity profiles among plots, we used Hill’s series, an equation that calculates different biodiversity indexes for the same dataset (Tóthmérész 1995). With the Hill index we compared these different indexes (e.g., species richness, Shannon, Simpson, evenness, etc.), which emphasize different ecological aspects, such as quantity of species, species dominance, and rarity of species. To compare floristic composition among plots, we carried out a hierarchical clustering analysis based on the presence-absence of all 230 ethnospecies and applied the Jaccard similarity index (Legendre and Legendre 2012a). To compare floristic structure among plots, we calculated the total basal area, ethnospecies density, and total abundance for each plot (Table 3). Analyses were performed using R v.3.6.0 software (R Core Team 2019; Appendix 2).

RESULTS

Zoʻé’s forest TEK

According to Zoʻé cosmology, animals and plants have volitions and interact through partnership, chieftainship, war, etc., so that what ecologists call ecological interactions the Zoʻé describe as social relations. For example, they say that the tapir (Tapirus terrestris) jiawu/calls the taman (a small hawk) to take its ticks off, as the taman is its ribe/pet; the agouti (Dasyprocta aguti) jaty/plants its flour (Brazil nut [Bertholletia excelsa]) and gets doryj/unhappy when the paca (Cuniculus paca) steals its food; the Harpy Eagle (Harpia harpyja) is juke ijet/chieftain at killing, because it hunts large animals, such as spider monkeys (Ateles sp.); certain trees (e.g., Cecropia sp.) ory/rejoice with other trees (e.g., Schefflera sp.) and help them to grow, thus promoting a pijã/partnership. Places where these and other social relations (involving humans and/or non-humans) occur represent tekoha/social territory, because the development of these relations promotes a tekoha, which is a place where beings grow their food, hunt, sleep, etc. For example, swiddens are part of the tekoha of the Zoʻé, but also of other non-humans that inhabit them, such as crops. Upland forest patches are the tekoha of spider monkeys, who understand large trees (e.g., Angelim [Dinizia excelsa]) as their kiha/hammock, but are also the tekoha of some Zoʻé groups because such forests include their hunting trails. Therefore, all beings have their own tekoha that are located in certain places, and these places are relational as they express an entanglement of tekoha of different beings according to their points of view (cf. de Castro 1998, de Oliveira 2016).

In this context, the Zoʻé describe forest succession as transformations of entanglements of human and non-human tekoha. Such transformations occur as social relations arise and disappear, and the tekoha of certain beings are transformed into others, so that the Zoʻé understand different forest successional stages as different tekoha entanglements. For example, they say that in their mature swiddens, reduced cassava manioc (Manihot esculenta) production results from the volition of the very crop who gets doryj/unhappy as its roots are perforated by flechal (Gynerium sagittatum), who want to establish their tekoha there. Over time, some trees (e.g., babake/Embaúba [Cecropia sp.]) and palms (e.g., takumã/Tukumã [Astrocaryum aculeatum]) expel the flechal, and other trees (e.g., tapery/Tapereba (Spondias mombin) and nã/Brazil nut) and palms (e.g., ijeja/Inajá [Attalea maripa]) sprout from Zoʻé dump heaps. These trees/palms attract rodents, small birds, and monkeys, who start to manifest their own social relations there. Then, kuduaru frogs (cf. Trachycephalus sp.) establish their tekoha in some hollow trees, and the tapir, being ory/happy with frog songs, defecates seeds next to these trees. Gradually, tekoha transformations occur as forest regrowth occurs.

The Zoʻé understand that tekoha transformations are the result not only of non-human volitions, but also of Zoʻé agency. Such understanding occurs because when the Zoʻé occupy a forest patch, they transform non-humans’ tekoha into their own tekoha. For example, as the Zoʻé implement practices of slashing and burning, non-human tekoha are transformed into human tekoha. In turn, when the Zoʻé fallow their swiddens, they make possible the establishment of non-human tekoha in that area. Therefore, Zoʻé mobility associated with the practice of opening and fallowing swiddens influences the existence of non-human tekoha transformations.

Along with seasonality and sociohistorical aspects, cosmological aspects also influence Zoʻé mobility and are central in determining local movements. In this sense, the Zoʻé say that the piji (the Zoʻé’s aroma) determines behaviors of approach/departure and precaution, both among the Zoʻé themselves and with other beings. For example, a hunter’s piji can attract or drive game away, and a newborn’s piji can attract predators, thus requiring their relatives not to work in their swiddens, hunt, or gather in order to protect the newborn. As the Zoʻé transform landscapes and establish villages and swiddens, their piji impregnates these areas and thus attracts game, mainly spider monkeys, who want to be pijã/partner of the Zoʻé. Nonetheless, when piji gets excessive in an area and the spider monkeys perceive that the Zoʻé want to kill them, what would be a partnership for the spider monkeys reveals itself to be a dipisi/war, and the spider monkeys become vindictive and can send diseases to hunters and their families. Because of these and other reactions of game, plants, and other beings, the Zoʻé consider moderation in their behaviors as an ethical principle. This moderation governs respect for social and territorial distances in relation to non-humans. After years of occupying a region, the relative scarcity of game leads the Zoʻé to temporarily vacate it to look for other regions where game, mainly spider monkeys, are not used to Zoʻé’s piji.

Besides landscape transformations for opening villages and swiddens, Zoʻé mobility also includes landscape transformations associated with opening of camps (sometimes on ancient villages) and fallow management. In these cases, they can hunt, gather, manage trees/palms, and harvest remnant crops. Camps are established by selecting small trees (DAP ≤ ~7 cm) for cutting in areas of ~250 m², so that the canopy remains. In some camps, we observed hundreds of ijeja/Inajá and patawá/Patauá (Oenocarpus bataua) seeds scattered on the ground by the Zoʻé, as well as fallow areas where remnant crops, such as pako/Banana (Musa sp.), kuj/Cuia (Crescentia cujete), and ruku/Urucum (Bixa orellana), remained because of the Zoʻé recurrently opening small gaps in the canopy. Close to these crops, we observed houseposts and pottery remnants of ancient occupations (Fig. 2). It is common that such camps and fallows contain a mix of pioneer and late succession trees, palms with edible fruits, and crops. According to the Zoʻé, their management practices influence the existence of this ethnospecies mixture in their camps/fallows that favors the existence of different game species in the forest patch so that the game start to establish their tekoha there.

The Zoʻé perspective that non-humans have their own tekoha, relate socially, and therefore can be vindictive reinforces respect and the need for distancing in relation to these non-humans. In this context, the Zoʻé understand forest management as the implementation of mobility associated with practices for opening/vacating forest patches, that ensures both the existence of different human and non-human tekoka, and certain distancing in relation to vindictive game. The foundation of the social-ecological relations that structure this understanding is the ethic of moderation, especially with game, among which the relationship with the spider monkey stands out, so that the search for fat game is the main driving force of Zoʻé mobility. At least during the last 140 years, such mobility has triggered landscape transformations that have made possible the existence of forest patches in different successional stages, in either old swidden-fallow or camping areas, such as the five areas we inventoried.

Impact of Zoʻé’s forest TEK on forest structure and alpha diversity

Values of total basal area and ethnospecies density in forest plots over 28 and ~70 years old, respectively, were similar to old-growth forests (Table 3). In old-growth forests, total basal area, ethnospecies density, and total abundance values varied. For example, in the old-growth forest ≥ 140b, values of these variables were similar to young forests (Table 3), although its ethnospecies relative abundance and composition remained similar to the old-growth forest ≥ 140c (Figs. 3 and 4).

Forest plots of ~70 and ≥ 140c years old showed the greatest values of species richness, and the nine-year-old forest plot the smallest value (Fig. 5). Species richness in the intermediate aged (~70 years old) forest plot was 27.5% and 14.7% higher than in the old-growth forests ≥ 140a and ≥ 140b, respectively (Fig. 5). Regarding diversity profiles, 28- and ~70-year-old forests show higher stability (i.e., lower curve slope that indicates greater floristic evenness and less dominance of abundant ethnospecies) than old-growth forests (Fig. 6). Diversity profiles also show the highest values of Shannon and Simpson indexes for the ~70-year-old forest plot (Fig. 6). Overall, these results show highest alpha diversity (i.e., local diversity) in the intermediate aged ~70-year-old forest plot.

Impact of Zoʻé’s forest TEK on beta diversity

Ordination of variation in ethnospecies relative abundance among plots by NMDS captured 83% of the variance in the original matrix and shows a floristic turnover across a gradient of successional stages related to forest patch ages (Fig. 3). This gradient shows that beta diversity (i.e., floristic variability among plots) is higher in landscapes with an ensemble of different successional stages than in old-growth forests alone. In these landscapes, young (nine and 17), intermediate (28, ~70, and ~140), and old-growth (> 140) forests are dominated by pioneer (e.g., nengansing, babake, and wire’i), secondary (e.g., tapery, buburu, and tura pirang), and late successional (e.g., rowa’y, kapu, and siri’y) ethnospecies, respectively (Fig. 3). Importantly, most of the useful ethnospecies found in our plots are secondary ethnospecies. In turn, landscapes dominated by old-growth forests are dominated mainly by late successional ethnospecies. Floristic composition also varied among plots, and composition of young and intermediate forests was distinct from old-growth forests (≥ 140b/≥ 140c isolated branch in Fig. 4), except the 28-year-old forest, which was similar to the old-growth forest ≥140a (Fig. 4). Floristic composition was related to forest age independently of proximity among plots (Fig. 1c; Table 2).

DISCUSSION

The Zoʻé perspective on forest management: sustainability within an ethic of moderation

A key aspect to understanding forest management is sustainability (McDonald et al. 2004, Gough et al. 2008). Indigenous understandings of sustainability are underpinned by sociocosmological aspects (Fernández-Llamazares and Virtanen 2020, Virtanen et al. 2020), so understanding their forest management requires considering their perspectives (Franco-Moraes et al. 2021). For example, among the Kaʻapor, from eastern Brazilian Amazonia, sustainability means implementing practices for opening/vacating forest patches mainly in response to a social-ecological relationship with a specific tortoise (Geochelone denticulata; Balée 1985). In the Zoʻé case, sustainability means producing their own tekoha/social territory (a concept present in many Tupi-Guarani speaking Indigenous Peoples; Mondardo 2019) through an ethic of moderation (cf. Lévi-Strauss 1968, Gallois 1988, Aparício 2020), i.e., through behaviors of decorum and precaution with non-humans (cf. Braga et al. 2020). This ethic results not only in the promotion of Zoʻé tekoha but also of non-human tekoha, so that it sustains biocultural diversity in Zoʻé landscapes: a sustainable world for the Zoʻé means a world in which human and non-human sociabilities thrive together. Therefore, social-ecological relationships (Winter et al. 2018) among the Zoʻé and non-humans allow the existence of these different non-human tekoha. It is in this context that Zoʻé forest management occurs, because the implementation of practices of opening/vacating forest patches, as well as of establishing camps and taking care of old-fallows, has sociocultural objectives associated with an ethic of moderation with non-humans, mainly spider monkeys.

The ethic of moderation with spider monkeys is justified by the Zoʻé because these monkeys are thought to be vindictive after recognizing the Zoʻé’s piji (i.e., the Zoʻé’s aroma). Therefore, sensible qualities associated with olfactory aspects are central in the interpretation of ecological processes associated with spider monkey behaviors, thus manifesting a “logic of sensible qualities” (cf. Lévi-Strauss 1962), in which aromas, pains, colors, flavors, sounds, and textures compose people’s systems of knowledge. Just as occurs in relation to cultivation, cooking, and couvade (Braga 2017, 2021b), the Zoʻé express an ethic of moderation in forest management through behaviors associated with such a logic. This suggests that among Amazonian Indigenous Peoples the ethic of moderation is not necessarily expressed through social-ecological relationships mediated by non-human masters (i.e., spiritual beings who own animals and plants; Fausto 2008, Fausto and Neves 2018), which implies that grounding notions of sustainability in mastery (Fernández-Llamazares and Virtanen 2020) is not as pervasive as has been thought. As we have shown, sustainability in Zoʻé management is ensured through an ethic of moderation associated with a logic of sensible qualities, even if relationships among the Zoʻé and animals, plants, and other beings are not mediated by non-human masters.

The Zoʻé perspective of forest management is based on an ethic of moderation, and the moderation with spider monkeys represents a keystone biocultural trait (cf. Winter et al. 2018) structuring such a perspective. To our knowledge, although some Amazonian Indigenous Peoples relate to spider monkeys in different ways (Cormier and Urbani 2008), this is the first study that shows that a keystone biocultural trait of moderation can structure many social-ecological relationships and forest management practices, therefore corroborating the hypothesis of Winter et al. (2018). This keystone biocultural trait could thus be used to further study the link between biological and cultural diversity using information entropy criteria (Reyes-Valdés and Kantartzi 2020).

Following the social-ecological framework proposed by Franco-Moraes et al. (2021), the Zoʻé perspective on forest management develops as follows: cosmological aspects (understanding that non-humans have social lives) ground a social-ecological relationship (moderation with spider monkeys) that guides practices (opening/vacating swiddens and camps). In turn, these practices are influenced by information about animals and plants (e.g., spider monkey behaviors) that are interpreted according to a logic of sensible qualities that is centered in olfactory attributes of ethnospecies. It is in this context that Zoʻé forest management promotes different tekoha entanglements in space-time, thus promoting landscape transformations that make possible the existence of forest patches in different successional stages.

Zoʻé forest management as a sustainable ecological disturbance promoting forest resilience

After 28 years, basal area in old swidden-fallow forest patches reached similar levels as that of old-growth forests (Table 3), thus suggesting forest biomass resilience after Zoʻé disturbances. Two reasons may contribute to such a recovery in Zoʻé landscapes: (i) local mobility associated with the opening and vacating of forest patches, thus avoiding land-use intensification (Jakovac et al. 2015); (ii) soil improvement because of old burning for opening swiddens (Franco-Moraes et al. 2019, Levis et al. 2020). Regarding ethnospecies density, our results show that after 17 years, secondary forests may have 70% of the ethnospecies density found in old-growth forests, indicating ethnospecies density resilience.

Secondary and old-growth forests had different floristic compositions in general (Fig. 4), although one old-growth forest plot (≥ 140a) had floristic composition similar to the 28-year-old forest plot. Whereas in secondary forests multiple successional trajectories can explain high floristic variability (Chazdon 2008, Norden et al. 2015), in old-growth forests natural small disturbances can allow colonization by secondary species, so that composition becomes similar to intermediate secondary forests (Chazdon 2003, Schietti et al. 2016). Natural disturbances are common in old-growth forests and may explain, for example, the variation in values of total basal area, ethnospecies density, and total abundance among these forests in our plots (Table 3), although they did not cause changes in the relative abundance of ethnospecies (Fig. 3).

Overall, these results suggest that Zoʻé management acts as a sustainable ecological disturbance (cf. Uhl et al. 1990, López-Zent and Zent 2004) by making possible the existence of resilient forest patches with ethnospecies compositions and abundances not found even in disturbed old-growth forests. From the Zoʻé’s perspective, this occurs because social relations among non-humans in old-swidden fallow areas are different from those in old-growth forests, a perspective also described for the Wajãpi from northeastern Amazonia (de Oliveira 2012).

Zoʻé ecological disturbances boost alpha and beta diversity

The intermediate ~70-year-old secondary forest shows the highest values of ethnospecies richness (together with the old-growth forest ≥ 140c; Fig. 5), Shannon and Simpson diversity indexes and ethnospecies evenness (Fig. 6), and a mixture of ethnospecies from young and old-growth forests (Fig. 3). These findings can result from the fact that intermediate successional forests contain opportunistic and competing species coexisting without dominance, which generates a lower degree of competitive exclusion, and thus higher floristic diversity (Connell 1978, Sheil and Burslem 2013). More broadly, our findings suggest that testing the intermediate disturbance hypothesis (IDH) is still a promising avenue (but see Fox 2013, Sheil and Burslem 2013, Barabaìs et al. 2018) to understand biodiversity in forest systems not only from an ecological perspective of disturbance intensity and frequency (Molino and Sabatier 2001, Svensson et al. 2012, Guitet et al. 2018), but also from a biocultural perspective of forest recovery time since the last human disturbance. Moreover, we call attention to the fact that disturbance is only one of the factors that can influence floristic diversity in tropical forests, because topography, dispersal limitation, and soil water availability, among others also influence floristic diversity (Bongers et al. 2009). These factors may explain, for example, the high value of ethnospecies richness found in the old-growth forest ≥ 140c, that made the curve in Figure 5b look bimodal and not unimodal as predicted by the IDH (cf. Johst and Huth 2005).

We also found that the Zoʻé’s sociocultural strategy of creating spatially heterogeneous successional stages at a landscape scale had a positive impact on beta diversity, because Zoʻé landscape transformations promote different ethnospecies compositions across these successional stages (Figs. 3 and 4). We can also interpret these results within the IDH framework at the landscape-scale, as landscapes with intermediate levels of disturbances are expected to have greater beta diversity (Solar et al. 2015). This occurs because beta diversity is low when the set of forest patches are either disturbed or undisturbed in similar ways, and reaches its maximal value when there is a set of forest patches containing both disturbed and undisturbed areas with different alpha diversities and compositions, each implying different recovery time since the last disturbance (Balée 2006, Guèze et al. 2015, Odonne et al. 2019). Overall, these results support previous calls to keep testing the impact of spatial disturbance regimes on beta diversity for ecological understanding (Solar et al. 2015), as well as for biocultural understanding (Maffi 2007).

Different ethnospecies compositions may have resulted not only from natural forest regrowth, but also from the influence of Zoʻé practices, such as scattering seeds, cutting trees, and opening gaps. Amazonian Indigenous Peoples have directly influenced species compositions and abundances through these practices (Ferreira et al. 2019, Franco-Moraes et al. 2019), which appears to have occurred in the Zoʻé case. For example, greater abundance of ethnospecies used as food in forests between 17 and 140 years old than in old-growth forests (Fig. 3) may be related to these practices, as expected from forest domestication (Levis et al. 2018, Flores and Levis 2021). The Zoʻé know the processes that promote this divergence in ethnospecies compositions and have interest in such promotion. However, although this promotion generates food, this interest does not represent an intention to domesticate the forest to produce food, instead, as we show, it is associated with cosmological aspects (cf. da Cunha 2019, Aparício 2020, Santos and Soares 2021), whose result is the emergence of domesticated forests (Levis et al. 2018).

We acknowledge that a greater number of chronosequence samples could further improve our understanding about the influence of Zoʻé landscape transformations on biodiversity. One of the most difficult tasks in chronosequence studies is figuring out the age of forest patches in advanced stages of succession, and, in fact, the lack of such information is one of the main reasons why chronosequence-based studies often deviate from long-term monitoring (Walker et al. 2010). In this sense, our study provides important empirical evidence rarely presented in chronosequence studies as we collected information about land use history and age of forest patches in advanced successional stages. Moreover, to our knowledge, this is the first study to show how sociocultural elements associated with Indigenous TEK (i.e., cosmologies, social relations, etc.) have influenced the promotion of floristic diversity in tropical forests.

Overall, our results are relevant to the Zoʻé because they highlight the importance of their socioculture for the promotion of local floristic diversity, thus showing the central role of Zoʻé TEK in local biodiversity conservation. More broadly, our results highlight how Indigenous forest disturbance regimes can be important for the maintenance or even enhancement of Amazonian floristic diversity, as well as for the resilience of local social-ecological systems.

Implications for biocultural conservation

Biocultural diversity includes biological and cultural diversity, which have coevolved together (Maffi 2007, Gavin et al. 2015), and are threatened by the same political-economic interests (Gorenflo et al. 2012, Aswani et al. 2018, Clement et al. 2020). Biocultural conservation requires acknowledging local perspectives that favor biodiversity according to their own understanding of what diversity is (Rozzi 2018). Here, by taking into account Zoʻé knowledge about floristic composition, we show that the Zoʻé perspective on forest management influences the promotion of floristic diversity, so that Zoʻé TEK leads to ecological outcomes that are expected from biocultural and ecological theories. In this sense, we argue that Indigenous TEK could be of importance for scientific theories that are frequently used to design conservation planning in social-ecological systems (Fernández-Llamazares and Cabeza 2018, Albuquerque et al. 2021). Especially in science assessments, where both the sustainability indicators that we use and how we do our biodiversity analyses influence the results that can be used in political decisions (Sterling et al. 2017), Indigenous TEK can contribute to test hypotheses and assess local outcomes of management practices without causing social injustice (Virtanen et al. 2020, Franco-Moraes et al. 2021).

In 2019, the Zoʻé created on their PGTA (Territorial and Environmental Management Plan; Iepé and FPEC 2019), which is an instrument of the Brazilian PNGATI (National Policy for Territorial and Environmental Management of Indigenous Lands). The Zoʻé PGTA defines guidelines to ensure Zoʻé’s territorial autonomy, physical/cultural reproduction, environmental sustainability, and food sovereignty according to Zoʻé perspectives. However, proper implementation of the PNGATI and other Indigenous public policies by the Brazilian government has not occurred (Testa et al. 2019), and Brazilian Indigenous Peoples have criticized such negligence (APIB 2019). Along with the PNGATI, other public policies that seek to empower Indigenous Peoples through local governance and stewardship (Ross et al. 2011, Artelle et al. 2019) are important not only from an Indigenous perspective, but also from a scientific perspective. Respecting Indigenous Peoples’ land rights and ensuring their governance have improved forests’ carbon storage (Stevens et al. 2014, Frechette et al. 2018) and conserved biodiversity (Corrigan et al. 2018, Schuster et al. 2019) worldwide. In this context, we hope that a better understanding of forest management from the Indigenous perspective—by scientists, conservationists, and policy makers—can enrich scientific knowledge, improve our ability to sustainably act on biocultural diversity, and promote social justice.

CONCLUSIONS

Zoʻé cosmological aspects underlie a forest management perspective that influences forest disturbance regimes that generate a sustainable social-ecological system. This occurs through the promotion of floristic diversity on both the local level (i.e., in forest patches of intermediate age) and landscape level (i.e., in landscapes with a set of disturbed and undisturbed forests). Zoʻé well-being and local forest resilience depend on these forest disturbance regimes, so that the sustainability of the Zoʻé social-ecological system is structured by sociocultural aspects that enable sustainable landscape management. We believe that Indigenous perspectives about forest management, which includes cosmological aspects, should be included in forest conservation efforts aimed at protecting Amazonian biocultural diversity (cf. Fernández-Llamazares and Virtanen 2020, Virtanen et al. 2020). Such inclusion should occur by considering local attitudes toward conservation (Kohler and Brondizio 2016), such as the Zoʻé forest disturbance regimes. The appreciation of these attitudes can guide inclusive and policy-relevant options for people and nature (cf. McElwee et al. 2020), thus generating resilient and sustainable social-ecological systems.

LITERATURE CITED

Albuquerque, U. P., D. Ludwig, I. S. Feitosa, J. M. B. de Moura, P. H. S. Gonçalves, R. H. da Silva, T. C. da Silva, T. Gonçalves-Souza, and W. S. Ferreira Júnior. 2021. Integrating traditional ecological knowledge into academic research at local and global scales. Regional Environmental Change 21:1-11. https://doi.org/10.1007/s10113-021-01774-2

Aparício, M. 2020. Contradomesticação na Amazônia indígena: a botânica da precaução. Pages 189-212 in J. Cabral-Oliveira, M. Amoroso, A. G. Morim de Lima, K. Shiratori, S. Marras, and L. Emperaire, editors. Vozes vegetais: diversidade, resistências e histórias da floresta. Ubu Editora, São Paulo, Brasil.

Artelle, K. A., M. Zurba, J. Bhattacharyya, D. E. Chan, K. Brown, J. Housty, and F. Moola. 2019. Supporting resurgent Indigenous-led governance: a nascent mechanism for just and effective conservation. Biological Conservation 240:108284. https://doi.org/10.1016/j.biocon.2019.108284

Articulação dos Povos Indígenas do Brasil (APIB). 2019. Resistimos há 519 anos e continuaremos resistindo. Mobilização Nacional Indígena. https://mobilizacaonacionalindigena.wordpress.com/2019/04/26/documento-final-do-xv-acampamento-terra-livre/

Aswani, S., A. Lemahieu, and W. H. H. Sauer. 2018. Global trends of local ecological knowledge and future implications. PLoS ONE 13(4):e0195440. https://doi.org/10.1371/journal.pone.0195440

Balée, W. 2006. The research program of historical ecology. Annual Review of Anthropology 35:75-98. https://doi.org/10.1146/annurev.anthro.35.081705.123231

Balée W., and A. Gély. 1989. Managed forest succession in Amazonia: the Kaʻapor case. Advances in Economic Botany 7:129-158.

Barabìs, G., R. D’Andrea, and S. M. Stump. 2018. Chesson’s coexistence theory. Ecological Monographs 88:277-303. https://doi.org/10.1002/ecm.1302

Berkes, F., J. Colding, and C. Folke. 2000. Rediscovery of traditional ecological knowledge as adaptive management. Ecological Applications 10:1251-1262. https://doi.org/10.1890/1051-0761(2000)010[1251:ROTEKA]2.0.CO;2

Bernard, H. R. 1988. Research methods in cultural anthropology. Sage, Newbury Park, California, USA.

Bongers, F., L. Poorter, W. D. Hawthorne, and D. Sheil. 2009. The intermediate disturbance hypothesis applies to tropical forests, but disturbance contributes little to tree diversity. Ecology Letters 12:798-805. https://doi.org/10.1111/j.1461-0248.2009.01329.x

Braga, L. V. 2017. Paniʻem: um esboço sobre os modos de saber entre os Zoʻé. Thesis. Universidade de São Paulo, São Paulo, Brazil.

Braga, L. V. 2021a. Eremiʻu rupa. Abrindo roças. Iepé/FPEC-FUNAI/Fundo de Artesanato Zoʻé-FAC, São Paulo, Brasil.

Braga, L. V. 2021b. Panem. Sobre seu viés de gênero entre os Zoʻé. Mana 27:1-30. https://doi.org/https://doi.org/10.1590/1678-49442021v27n2a201

Braga, L. V., H. P. S. Pedreira, and F. D. Cabalzar. 2020. Fazer saber a própria terra. Pages 133-165 in N. R. Moraes, L. A. Baptaglin, L. E. Vilella, A. C. Campos, and R. F. Azerêdo, editors. Povos originários e comunidades tradicionais: trabalhos de pesquisa e de extensão universitária, vol. 4. Fi, Porto Alegre, Brasil.

Chazdon, R. L. 2003. Tropical forest recovery: legacies of human impact and natural disturbances. Perspectives in Plant Ecology, Evolution and Systematics 6:51-71. https://doi.org/10.1078/1433-8319-00042

Chazdon, R. L. 2008. Chance and determinism in tropical forest succession. Pages 384-408 in W. P. Carlson, and S. A. Schnitzer, editors. Tropical forest community ecology. Blackwell, Hoboken, New Jersey, USA.

Chazdon, R. L. 2014. Tropical forest dynamics and disturbance regimes. Pages 55-72 in Second growth: the promise of tropical forest regeneration in an age of deforestation. The University of Chicago Press, Chicago, Illinois, USA. https://doi.org/10.7208/chicago/9780226118109.003.0004

Clement, C. R., C. Levis, J. Franco-Moraes, and A. B. Junqueira. 2020. Domesticated nature: the culturally constructed niche of humanity. Pages 35-51 in C. Baldalf, editor. Participatory biodiversity conservation: concepts, experiences, and perspectives. Springer, Cham, Switzerland. https://doi.org/10.1007/978-3-030-41686-7_3

Connell, J. H. 1978. Diversity in tropical rain forests and coral reefs: high diversity of trees and corals is maintained only in a nonequilibrium state. Science 199:1302-1310. https://doi.org/10.1126/science.199.4335.1302

Cormier, L. A., and B. Urbani. 2008. The ethnoprimatology of spider monkeys (Ateles spp.): from past to present. Pages 377-403 in C. J. Campbell, editor. Spider monkeys: behavior, ecology and evolution of the genus Ateles. Cambridge University Press, Cambridge, UK. https://doi.org/10.1017/CBO9780511721915.014

Corrigan, C., H. Bingham, Y. Shi, E. Lewis, A. Chauvenet, and N. Kingston. 2018. Quantifying the contribution to biodiversity conservation of protected areas governed by Indigenous peoples and local communities. Biological Conservation 227:403-412. https://doi.org/10.1016/j.biocon.2018.09.007

Coscieme, L., H. da Silva Hyldmo, Á. Fernández-Llamazares, I. Palomo, T. H. Mwampamba, O. Selomane, N. Sitas, P. Jaureguiberry, Y. Takahasi, M. Lim, M. P. Barral, J. S. Farinaci, J. Diaz-José, S. Ghosh, J. Ojino, A. Alassaf, B. N. Baatuuwie, L. Balint, Z. Basher, F. Boeraeve, S. Budiharta, R. Chen, M. Desrousseaux, G. Dowo, C. Febria, H. Ghazi, Z. V. Harmáčková, R. Jaffe, M. M. Kalemba, C. K. Lambini, F. P. S. Lasmana, A. A. A. Mohamed, A. Niamir, P. Pliscoff, R. Sabyrbekov, U. B. Shrestha, A. Samakov, A. A. Sidorovich, L. Thompson, and M. Valle. 2020. Multiple conceptualizations of nature are key to inclusivity and legitimacy in global environmental governance. Environmental Science & Policy 104:36-42. https://doi.org/10.1016/j.envsci.2019.10.018

da Cunha, M. C. 2017. Traditional people, collectors of diversity. Pages 257-272 in M. Brightman, and J. Lewis, editors. The anthropology of sustainability. Palgrave Macmillan, New York, New York, USA. https://doi.org/10.1057/978-1-137-56636-2_15

da Cunha, M. 2019. Antidomestication in the Amazon: swidden and its foes. HAU: Journal of Ethnographic Theory 9:126-136. https://doi.org/10.1086/703870

Datta, R. 2015. A relational theoretical framework and meanings of land, nature, and sustainability for research with Indigenous communities. Local Environment 20:102-113. https://doi.org/10.1080/13549839.2013.818957

de Castro, E. 1998. Cosmological deixis and Amerindian perspectivism. Journal of the Royal Anthropological Institute 4:469-488. https://doi.org/10.2307/3034157

de Oliveira, J. 2012. Entre plantas e palavras. Modos de constituição dos saberes entre os Wajãpi (AP). Thesis. Universidade de São Paulo, São Paulo, Brazil.

de Oliveira, J. 2016. Worlds of gardens and forests. Boletim do Museu Paraense Emílio Goeldi: Ciências Humanas 11:115-131. https://doi.org/https://doi.org/10.1590/1981.81222016000100007

de Oliveira, J. 2019. A sedução das mandiocas. Pages 73-85 in B. C. Labate, and S. L. Goulart, editors. O uso de plantas psicoativas nas Américas. Gramma, Rio de Janeiro, Brasil.

Denevan, W. M. 2001. Cultivated landscapes of native Amazonia and the Andes. Oxford University Press, Oxford, UK.

Descola, P. 2005. Ecology as cosmological analysis. Pages 22-35 in A. Surrallés, and P. G. Hierro, editors. The land within: Indigenous territory and the perception of the environment. IWGIA, Copenhagen, Denmark.

Douterlungne D., S. I. Levy-Tacher, D. J. Golicher, and F. R. Dañobeytia. 2010. Applying Indigenous knowledge to the restoration of degraded tropical rain forest clearings dominated by bracken fern. Restoration Ecology 18:322-329. https://doi.org/10.1111/j.1526-100X.2008.00459.x

Emperaire, L. 2005. A biodiversidade agrícola na Amazônia brasileira: recurso e patrimônio. Revista do Patrimônio Histórico e Artístico Nacional 32:31-43.

Emperaire, L., P. G. Bustamante, C. Fausto, F. Freitas, G. Mendes, and M. Smith. Agrobiodiversidade e roças. 2021. Pages 18-56 in M. C. da Cunha, S. B. Magalhães, and C. Adams, editors. Povos tradicionais e biodiversidade no Brasil—contribuições dos povos indígenas, quilombolas e comunidades tradicionais para a biodiversidade, políticas e ameaças, vol. 7. SBPC, São Paulo, Brasil.

Faith, D. P., P. R. Minchin, and L. Belbin. 1987. Compositional dissimilarity as a robust measure of ecological distance. Vegetatio 69:57-68. https://doi.org/10.1007/BF00038687

Fausto, C. 2008. Too many owners: mastery and ownership in Amazonia. Mana 19:329-366. https://doi.org/10.1590/S0104-93132008000200003

Fausto, C. 2019. La diversité en petits intervalles: logique de variation en Amazonie. Pages 315-328 in G. Cometti, P. Le Roux, T. Manicone, and N. Martin, editors. Au seuil de la forêt. Hommage à Philippe Descola, l’anthropologue de la nature. Tautem, Strasbourg, France.

Fausto, C., and E. G. Neves. 2018. Was there ever a Neolithic in the Neotropics? Plant familiarisation and biodiversity in the Amazon. Antiquity 92:1604-1618. https://doi.org/10.15184/aqy.2018.157

Fernández-Llamazares, Á., and M. Cabeza. 2018. Rediscovering the potential of Indigenous storytelling for conservation practice. Conservation Letters 11:e12398. https://doi.org/10.1111/conl.12398

Fernández-Llamazares, Á., and P. K. Virtanen. 2020. Game masters and Amazonian Indigenous views on sustainability. Current Opinion in Environmental Sustainability 43:21-27. https://doi.org/10.1016/j.cosust.2020.01.004

Ferreira, M. J., C. Levis, J. Iriarte, and C. R. Clement. 2019. Legacies of intensive management in forests around pre-columbian and modern settlements in the Madeira-Tapajós interfluve, Amazonia. Acta Botanica Brasilica 33:212-220. https://doi.org/10.1590/0102-33062018abb0339

Finegan, B. 1996. Pattern and process in neotropical secondary rain forests: the first 100 years of succession. Trends in Ecology & Evolution 11:119-124. https://doi.org/https://doi.org/10.1016/0169-5347(96)81090-1

Flores, B. M., and C. Levis. 2021. Human-food feedback in tropical forests. Science 372:1146-1147. https://doi.org/10.1126/science.abh1806

Food and Agriculture Organization of the United Nations (FAO). 2022. Forest management planning. Sustainable forest management (SFM) toolbox. FAO, Rome, Italy. http://www.fao.org/sustainable-forest-management/toolbox/modules/forest-management-planning/basic-knowledge/en/

Fox, J. 2013. The intermediate disturbance hypothesis should be abandoned. Trends in Ecology & Evolution 28:86-92. https://doi.org/10.1016/j.tree.2012.08.014

Franco-Moraes, J. 2021. Sucessão florestal e o manejo indígena na Amazônia brasileira. Pages 227-229 in M. Carneiro da Cunha, S. B. Magalhães, and C. Adams, editors. Povos tradicionais e biodiversidade no Brasil—contribuições dos povos indígenas, quilombolas e comunidades tradicionais para a biodiversidade, políticas e ameaças. v.7. SBPC, São Paulo, Brasil.

Franco-Moraes, J., A. F. M. B. Baniwa, F. R. C. Costa, H. P. Lima, C. R. Clement, and G. H. Shepard Jr. 2019. Historical landscape domestication in ancestral forests with nutrient-poor soils in northwestern Amazonia. Forest Ecology and Management 446:317-330. https://doi.org/10.1016/j.foreco.2019.04.020

Franco-Moraes, J., C. R. Clement, J. C. de Oliveira, and A. A. de Oliveira. 2021. A framework for identifying and integrating sociocultural and environmental elements of Indigenous peoples’ and local communities’ landscape transformations. Perspectives in Ecology and Conservation 19:143-152. https://doi.org/10.1016/j.pecon.2021.02.008

Frechette, A., C. Ginsburg, W. Walker, S. Gorelik, S. Keene, C. Meyer, K. Reytar, and P. Veit. 2018. A global baseline of carbon storage in collective lands. Rights and Resources Initiative, Washington, D.C., USA.

Gallois, D. T. 1988. Movimento na cosmologia waiapi: criação, expansão e transformação do universo. Thesis. Universidade de São Paulo, São Paulo, Brazil.

Gallois, D. T., H. P. da Silva Pedreira, and L. V. Braga. 2020. Construindo um Plano de Gestão Territorial e Ambiental com os Zo’é. Pages 108-131 in L. D. B. Grupioni, editor. Em busca do bem viver. Experiências de elaboração de Planos de Gestão Territorial e Ambiental de Terras Indígenas. Rede de Cooperação Amazônica, São Paulo, Brasil.

Gavin, M. C., J. McCarter, A. Mead, F. Berkes, J. R. Stepp, D. Peterson, and R. Tang. 2015. Defining biocultural approaches to conservation. Trends in Ecology & Evolution 30:140-145. https://doi.org/10.1016/j.tree.2014.12.005

Gómez-Pompa, A. 1987. On Maya silviculture. Mexican Studies/Estudios Mexicanos 3:1-17. https://doi.org/10.2307/4617029

Gordon, J. E., and A. C. Newton. 2006. The potential misapplication of rapid plant diversity assessment in tropical conservation. Journal for Nature Conservation 14:117-126. https://doi.org/10.1016/j.jnc.2006.01.001

Gorenflo, L. J., S. Romaine, R. A. Mittermeier, and K. Walker-Painemilla. 2012. Co-occurrence of linguistic and biological diversity in biodiversity hotspots and high biodiversity wilderness areas. Proceedings of the National Academy of Sciences 109:8032-8037. https://doi.org/10.1073/pnas.1117511109

Gotelli, N. J., and R. K. Colwell. 2001. Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecology Letters 4:379-391. https://doi.org/10.1046/j.1461-0248.2001.00230.x

Gough, A. D., J. L. Innes, and S. D. Allen. 2008. Development of common indicators of sustainable forest management. Ecological Indicators 8:425-430. https://doi.org/10.1016/j.ecolind.2007.03.001

Guèze, M., A. C. Luz, J. Paneque-Gálvez, M. J. Macía, M. Orta-Martínez, J. Pino, and V. Reyes-García. 2015. Shifts in Indigenous culture relate to forest tree diversity: a case study from the Tsimaneʻ, Bolivian Amazon. Biological Conservation 186:251-259. https://doi.org/10.1016/j.biocon.2015.03.026

Guitet, S., D. Sabatier, O. Brunaux, P. Couteron, T. Denis, V. Freycon, S. Gonzalez, B. Hérault, G. Jaouen, J. -F. Molino, R. Pélissier, C. Richard-Hansen, and G. Vincent. 2018. Disturbance regimes drive the diversity of regional floristic pools across Guianan rainforest landscapes. Scientific Reports 8:1-12. https://doi.org/https://doi.org/10.1038/s41598-018-22209-9

Havt, N. 2001. Representações do ambiente e da territorialidade entre os Zo’é/PA. Thesis. Universidade de São Paulo, São Paulo, Brazil.

Hill, R., G. Nates-Parra, J. J. G. Quezada-Euán, D. Buchori, G. LeBuhn, M. M. Maués, P. L. Pert, P. K. Kwapong, S. Saeed, S. J. Breslow, M. C. da Cunha, L. V. Dicks, L. Galetto, M. Gikungu, B. G. Howlett, V. L. Imperatriz-Fonseca, P. O’B. Lyver, B. Martín-López, E. Oteros-Rozas, S. G. Potts, and M. Roué. 2019. Biocultural approaches to pollinator conservation. Nature Sustainability 2:214-222. https://doi.org/10.1038/s41893-019-0244-z

Iepé, Instituto de Pesquisa e Formação Indígena, and FPEC, Frente de Proteção Etnoambiental Cuminapanema. 2019. Jo’e rekoha bokituteha ram: planejando como vamos continuar vivendo bem no futuro - Plano de Gestão Territorial e Ambiental da TI Zo’é. Iepé, São Paulo, Brasil.

Instituto Nacional de Meteorologia (INMET). 2020. INMET, Setor Sudoeste, Brasil. http://www.inmet.gov.br/portal/

Jakovac, C. C., M. Peña-Claros, T. W. Kuyper, and F. Bongers. 2015. Loss of secondary-forest resilience by land-use intensification in the Amazon. Journal of Ecology 103:67-77. https://doi.org/10.1111/1365-2745.12298

Johst, K., and A. Huth. 2005. Testing the intermediate disturbance hypothesis: when will there be two peaks of diversity? Diversity and Distributions 11:111-120. https://doi.org/https://doi.org/10.1111/j.1366-9516.2005.00133.x

Kettle, C. J. 2012. Seeding ecological restoration of tropical forests: priority setting under REDD+. Biological Conservation 154:34-41. https://doi.org/10.1016/j.biocon.2012.03.016

Kitamura, S. 2011. Frugivory and seed dispersal by Hornbills (Bucerotidae) in tropical forests. Acta Oecologica 37:531-541. https://doi.org/10.1016/j.actao.2011.01.015

Kohler, F., and E. S. Brondizio. 2017. Considering the needs of Indigenous and local populations in conservation programs. Conservation Biology 31:245-251. https://doi.org/10.1111/cobi.12843

Lawrence, D., C. Radel, K. Tully, B. Schmook, and L. Schneider. 2010. Untangling a decline in tropical forest resilience: constraints on the sustainability of shifting cultivation across the globe. Biotropica 42:21-30. https://doi.org/10.1111/j.1744-7429.2009.00599.x

Legendre, P., and L. Legendre. 2012a. Ecological resemblance. Pages 265-336 in Numerical ecology, third edition. Elsevier, Amsterdam, The Netherlands. https://doi.org/https://doi.org/10.1016/B978-0-444-53868-0.50007-1

Legendre, P., and L. Legendre. 2012b. Cluster analysis. Pages 337-424 in Numerical ecology, third edition. Elsevier, Amsterdam, The Netherlands. https://doi.org/https://doi.org/10.1016/B978-0-444-53868-0.50008-3

Levis, C., B. M. Flores, P. A. Moreira, B. G. Luize, R. P. Alves, J. Franco-Moraes, J Lins, E. Konings, M. Peña-Claros, F. Bongers, F. R. C. Costa, and C. R. Clement. 2018. How people domesticated Amazonian forests. Frontiers in Ecology and Evolution 5:171. https://doi.org/10.3389/fevo.2017.00171

Levis, C., M. Peña-Claros, C. R. Clement, F. R. C. Costa, R. P. Alves, M. J. Ferreira, C. G. Figueiredo, and F. Bongers. 2020. Pre-Columbian soil fertilization and current management maintain food resource availability in old-growth Amazonian forests. Plant and Soil 450:29-48. https://doi.org/10.1007/s11104-020-04461-z

Lévi-Strauss, C. 1962. The savage mind. University of Chicago, Chicago, Illinois, USA.

Lévi-Strauss, C. 1968. Mythologiques III: '’Origine des manières de table. Librairie Plon, Paris, France.

Link, A., and A. Di Fiore. 2006. Seed dispersal by spider monkeys and its importance in the maintenance of neotropical rain-forest diversity. Journal of Tropical Ecology 22:235-246. https://doi.org/10.1017/S0266467405003081

Loh, J., and D. Harmon. 2005. A global index of biocultural diversity. Ecological Indicators 5:231-241. https://doi.org/10.1016/j.ecolind.2005.02.005

López-Zent, E., and S. Zent. 2004. Amazonian Indians as ecological disturbance agents: the Hotï of the Sierra de Maigualida, Venezuelan Guayana. Advances in Economic Botany 15:79-112.

Maffi, L. 2007. Biocultural diversity and sustainability. Pages 267-77 in J. Pretty, T. Benton, J. Guivant, D. R. Lee, D. Orr, M. J. Pfeffer, and H. Ward, editors. The SAGE handbook on environment and society. SAGE, London, UK. https://sk.sagepub.com/reference/hdbk_envirosociety/n18.xml#:~:text=https%3A//dx.doi.org/10.4135/9781848607873.n18

McCune, B., and J. B. Grace. 2002. Nonmetric multidimensional scaling. Pages 125-142 in Analysis of ecological communities. Wild Blueberry Media, Corvallis, Oregon, USA.

McDonald, G. T., and M. B. Lane. 2004. Converging global indicators for sustainable forest management. Forest Policy and Economics 6:63-70. https://doi.org/10.1016/S1389-9341(02)00101-6

McElwee, P., Á. Fernández-Llamazares, Y. Aumeeruddy-Thomas, D. Babai, P. Bates, K. Galvin, M. Guèze, J. Liu, Z. Molnár, H. T. Ngo, V. Reyes-García, R. R. Chowdhury, A. Samakov, U. B. Shrestha, S. Díaz, and E. S. Brondízio. 2020. Working with Indigenous and local knowledge (ILK) in large-scale ecological assessments: reviewing the experience of the IPBES Global Assessment. Journal of Applied Ecology 57:1666-1676. https://doi.org/10.1111/1365-2664.13705

Mesquita, R. D. C. G., P. E. D. S. Massoca, C. C. Jakovac, T. V. Bentos, and G. B. Williamson. 2015. Amazon rain forest succession: stochasticity or land-use legacy? BioScience 65:849-861. https://doi.org/10.1093/biosci/biv108

Molino, J. F., and D. Sabatier. 2001. Tree diversity in tropical rain forests: a validation of the intermediate disturbance hypothesis. Science 294:1702-1704. https://doi.org/10.1126/science.1060284

Mondardo, M. 2019. Tekoha: lutas indígenas pelo território. EdUFRR, Roraima, Brasil.

Mukul, S. A., J. Herbohn, and J. Firn. 2020. Rapid recovery of tropical forest diversity and structure after shifting cultivation in the Philippines uplands. Ecology and Evolution 10:7189-7211. https://doi.org/10.1002/ece3.6419

Nikinmaa, L., M. Lindner, E. Cantarello, A. S. Jump, R. Seidl, G. Winkel, and B. Muys. 2020. Reviewing the use of resilience concepts in forest sciences. Current Forestry Reports 6:61-80. https://doi.org/10.1007/s40725-020-00110-x

Norden, N., H. A. Angarita, F. Bongers, M. Martínez-Ramos, I. Granzow-de la Cerda, M. van Breugel, E. Lebrija-Trejos, J. A. Meave, J. Vandermeer, G. B. Williamson, B. Finegan, R. Mesquita, and R. L. Chazdon. 2015. Successional dynamics in Neotropical forests are as uncertain as they are predictable. Proceedings of the National Academy of Sciences 112:8013-8018. https://doi.org/10.1073/pnas.1500403112

Odonne, G., M. van den Bel, M. Burst, O. Brunaux, M. Bruno, E. Dambrine, D. Davy, M. Desprez, J. Engel, B. Ferry, V. Freycon, P. Grenand, S. Jérémie, M. Mestre, J.-F. Molino, P. Petronelli, D. Sabatier, and B. Hérault. 2019. Long-term influence of early human occupations on current forests of the Guiana Shield. Ecology 100:e02806. https://doi.org/10.1002/ecy.2806

Oliveira, M. M., N. Higuchi, C. H. Celes, and F. G. Higuchi. 2014. Tamanho e formas de parcelas para inventários florestais de espécies arbóreas na Amazônia central. Ciência Florestal 24:645-653. https://doi.org/10.5902/1980509815744

Perrault-Archambault, M., and O. T. Coomes. 2008. Distribution of agrobiodiversity in home gardens along the Corrientes River, Peruvian Amazon. Economic Botany 62:109-126. https://doi.org/10.1007/s12231-008-9010-2

Phillips, O. L., and A. H. Gentry. 1993. The useful plants of Tambopata, Peru: II. Additional hypothesis testing in quantitative ethnobotany. Economic Botany 47:33-43. https://doi.org/10.1007/BF02862204

Pires, J. M., and G. T. Prance. 1985. The vegetation types of the Brazilian Amazon. Pages 109-145 in G. T. Prance, and T. E. Lovejoy, editors. Key environments: Amazonia. Elsevier Science & Technology, Oxford, UK.

Poffenberger, M., and B. McGean. 1993. Communities and forest management in east Kalimantan: pathway to environmental stability. Center for Southeast Asia Studies, University of California, Berkeley, California, USA.

Prance, G. T., W. Balee, B. M. Boom, and R. L. Carneiro. 1987. Quantitative ethnobotany and the case for conservation in Amazonia. Conservation Biology 1:296-310. https://doi.org/10.1111/j.1523-1739.1987.tb00050.x

R Core Team. 2019. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/

Reyes-Valdés, M. H., and S. K. Kantartzi. 2020. An information theory approach to biocultural complexity. Scientific Reports 10:1-8. https://doi.org/10.1038/s41598-020-64260-5

Rival, L., and D. McKey. 2008. Domestication and diversity in manioc (Manihot esculenta Crantz ssp. esculenta, Euphorbiaceae). Current Anthropology 49:1119-1128. https://doi.org/10.1086/593119

Ross, A., K. Pickering, J. G. Snodgrass, H. D. Delcore, and R. Sherman. 2011. Indigenous peoples and the collaborative stewardship of nature: knowledge binds and institutional conflicts. Left Coast Press, Walnut Creek, California, USA. https://doi.org/10.4324/9781315426617

Rozzi, R. 2018. Biocultural conservation and biocultural ethics. Pages 303-314 in R. Rozzi, R. H. May Jr., F. S. Chapin III, F. Massardo, M. C. Gavin, I. J. Klaver, A. Pauchard, M. A. Nuñez, and D. Simberloff, editors. Biocultural homogenization to biocultural conservation. Springer, Cham, Switzerland. https://doi.org/10.1007/978-3-319-99513-7_19

Saldarriaga, J. G., D. C. West, M. L. Tharp, and C. Uhl. 1988. Long-term chronosequence of forest succession in the Upper Rio Negro of Colombia and Venezuela. Journal of Ecology 76:938-958. https://doi.org/10.2307/2260625

Santos, G. M., and G. H. Soares. 2021. Amazônia indomável: relações fora do alcance da domesticação. Mundo Amazónico 12:e89601. https://doi.org/https://doi.org/10.15446/ma.v12n1.89601

Schietti, J., D. Martins, T. Emilio, P. F. Souza, C. Levis, F. B. Baccaro, J. L. P. da Veiga Pinto, G. M. Moulatlet, S. C. Stark, K. Sarmento, R. N. O. de Araújo, F. R. C. Costa, J. Schöngart, C. A. Quesada, S. R. Saleska, J. Tomasella, and W. E. Magnusson. 2016. Forest structure along a 600 km transect of natural disturbance and seasonality gradients in central-southern Amazonia. Journal of Ecology 104:1335-1346. https://doi.org/10.1111/1365-2745.12596

Schuster, R., R. R. Germain, J. R. Bennett, N. J. Reo, and P. Arcese. 2019. Vertebrate biodiversity on Indigenous-managed lands in Australia, Brazil, and Canada equals that in protected areas. Environmental Science & Policy 101:1-6. https://doi.org/10.1016/j.envsci.2019.07.002

Sheil, D., and D. F. R. P. Burslem. 2013. Defining and defending Connell’s intermediate disturbance hypothesis: a response to Fox. Trends in Ecology & Evolution 28:571-572. https://doi.org/https://doi.org/10.1016/j.tree.2013.07.006

Solar, R. R. C., J. Barlow, J. Ferreira, E. Berenguer, A. C. Lees, J. R. Thomson, J. Louzada, M. Maués, N. G. Moura, V. H. F. Oliveira, J. C. M. Chaul, J. H. Schoereder, I. C. Guimarães Vieira, R. Mac Nally, and T. A. Gardner. 2015. How pervasive is biotic homogenization in human-Zmodified tropical forest landscapes? Ecology Letters 18:1108-1118. https://doi.org/10.1111/ele.12494

Sterk, M., I. A van de Leemput, and E. T. H. M. Peeters. 2017. How to conceptualize and operationalize resilience in socio-ecological systems? Current Opinion in Environmental Sustainability 28:108-113. https://doi.org/https://doi.org/10.1016/j.cosust.2017.09.003

Sterling, E. J., C. Filardi, A. Toomey, A. Sigouin, E. Betley, N. Gazit, J. Newell, S. Albert, D. Alvira, N. Bergamini, et al. 2017. Biocultural approaches to well-being and sustainability indicators across scales. Nature Ecology and Evolution 1:1798-1806. https://doi.org/10.1038/s41559-017-0349-6

Stevens, C., R. Winterbottom, J. Springer, and K. Reytar. 2014. Securing rights, combating climate change: how strengthening community forest rights mitigates climate change. World Resources Institute, Washington, D.C., USA.

Svensson, J. R., M. Lindegarth, P. R. Jonsson, and H. Pavia. 2012. Disturbance-diversity models: what do they really predict and how are they tested? Proceedings of the Royal Society B: Biological Sciences 279:2163-2170. https://doi.org/https://doi.org/10.1098/rspb.2011.2620

Tengö, M., E. S. Brondizio, T. Elmqvist, P. Malmer, and M. Spierenburg. 2014. Connecting diverse knowledge systems for enhanced ecosystem governance: the multiple evidence base approach. Ambio 43:579-591. https://doi.org/10.1007/s13280-014-0501-3

Testa, A. Q., A. Clistenes, A. da Cruz, A. R. G. B. Proenç, and G. H. Shepard Jr. 2019. Crisis in the Amazon. New York Review of Books 66:46-46.

Tóthmérész, B. 1995. Comparison of different methods for diversity ordering. Journal of Vegetation Science 6:283-290. https://doi.org/10.2307/3236223

Uhl, C., D. Nepstad, R. Buschbacher, K. Clark, B. Kauffman, and S. Subler. 1990. Studies of ecosystem response to natural and anthropogenic disturbances provide guidelines for designing sustainable land-use systems in Amazonia. Pages 24-42 in A. B. Anderson, editor. Alternatives to deforestation: steps toward sustainable use of the Amazon rain forest. Columbia University Press, New York, New York, USA.

Venturieri, A., O. S. Watrin, M. A. Valente, A. G. S. Campos, and P. B. Silva Neto. 2000. Zoneamento agroecológico nas terras quilombolas Trombetas e Erepecuru. ARQMO-Comissão Pró-Índio de São Paolo, São Paulo, Brasil.

Villa, P. M., S. V. Martins, S. N. de Oliveira Neto, A. C. Rodrigues, L. G. Martorano, L. D. Monsanto, N. M. Cancio, and M. Gastauer. 2018. Intensification of shifting cultivation reduces forest resilience in the northern Amazon. Forest Ecology and Management 430:312-320. https://doi.org/10.1016/j.foreco.2018.08.014

Virtanen, P. K., L. Siragusa, and H. Guttorm. 2020. Introduction: toward more inclusive definitions of sustainability. Current Opinion in Environmental Sustainability 43:77-82. https://doi.org/10.1016/j.cosust.2020.04.003

Walker, L. R., D. A. Wardle, R. D. Bardgett, and B. D. Clarkson. 2010. The use of chronosequences in studies of ecological succession and soil development. Journal of Ecology 98:725-736. https://doi.org/10.1111/j.1365-2745.2010.01664.x

Whittaker, R. H. 1967. Gradient analysis of vegetation. Biological Reviews 49:207-264. https://doi.org/10.1111/j.1469-185X.1967.tb01419.x

Winter, K. B., N. K. Lincoln, and F. Berkes. 2018. The social-ecological keystone concept: a quantifiable metaphor for understanding the structure, function, and resilience of a biocultural system. Sustainability 10:3294. https://doi.org/10.3390/su10093294