The Labino community is located in the municipality of Ilha Grande in Piauí State (PI), and is separated from the municipality of Parnaíba (2°51'02" S and 41°46'26" W) by the PI-116 state highway. The municipality of Ilha Grande had a population (in 2015) of approximately 9211 (Institudo Brasileiro de Geografia Estatística [IBGE], 2015), and the local Residents Association indicated that the Labino community is composed of 200 families and approximately 400 residents. The community is located within the Parnaiba Delta Environmental Protection Area (APA) – created by Federal Decree no. 99.274 on August 28, 1996; the APA comprises the entire coastline of Piauí State, as well as parts of the states of Maranhão and Ceara (Figure 1). The Parnaíba Delta APA was created to protect the mouths of the Ubatuba, Timonha, and Parnaíba rivers, improve the quality of life of resident populations by orienting and disciplining local economic activities, foment ecological tourism and environmental education, and preserve local cultures and traditions (Vieira & Loiola, 2014). The regional climate is type Aw by the Koppen classification system, with a rainy season from January to June and a dry season from July through December (Bastos, Andrade Junior, & Rodrigues, 2011). The vegetation is typical regional "restinga", composed of a mosaic of three basic vegetation formations: open field (campestre), shrub, and arboreal (Santos-Filho, Almeida Jr, Soares, & Zickel, 2010).

Figure 1
Location of the study area - Labino community between the Municipalities of Ilha Grande and Parnaíba , PI, Brazil.

Data were collected during the period between November/2015 and January/2016. Similar to other ethnozoological studies (Alves et al., 2013; Alves & Souto, 2015; Van Den Bergh, Kusters, & Dietz, 2013), the investigations were undertaken using semi-structured questionnaires that included questions concerning: the socio-economic lives of the interviewees; their perceptions of the importance of the local avifauna, and the identification of local species.

One hundred and fifty local residents were interviewed, representing 37.5% of the focal population; the selection criteria was individuals older than 18. The sampling error was calculated to be 5%, with a 95% confidence interval (Bernard, 1988). To avoid biasing the information solicited (Albuquerque, Cunha, Lucena, & Alves, 2014), all of the interviews were held individually. Before each interview, the interviewees were asked to sign a Consent Form (TCLE) indicating their understanding of the project and free choice in participating. The present study was approved by the Research with Humans Ethics Committee of the Universidade Federal do Piauí – Campus Parnaíba (registry number 1.323.297).

The birds mentioned by the interviewees were identified to the species level using a field guide (Ridgely & Tudor, 1994; Sigrist, 2009). The taxonomic names are according to the determinations of the Brazilian Committee of Ornithological Registration for Birds (CBRO) (Piacentini et al., 2015); vernacular names follow, as provided by members of the community investigated.

The data were organized into digital archives (MS EXCEL© 2016) and the graphs were prepared at high resolution (300 dpi) with the aid of the DANIEL’s XL TOOLBOX, version 6.60 add-on open source tool (Kraus, 2014). The data were analyzed using univariate statistics to verify the existence of influences by socioeconomic factors on local ethno-ornithological knowledge. Statistical analyses were performed using SPSS^© version 23 software (IBM^© Corp., 2014), consistently using a significance level of 5% (p < 0.05).

The sample population was composed of 150 interviewees (51% men [n = 76] and 49% women [n = 74]); their ages varied from 18 to 87. In general, participant schooling levels were quite low, with 11.33% (n = 17) being illiterate while 40.67% did not complete grammar school. Family incomes in the Labino community varied between 1 and 4 minimum wages (the Brazilian minimum wage in May 2016 was ~ USD $248), but most of the informants (n=92; 61%) earned approximately 1 to 2 minimum wages. The municipality of Ilha Grande had a mean human development index (MHDI) of 0.563 in 2010. The gap between the MHDI of the municipality and the maximum value of that index (1.0) was reduced by 73.45% between 2000 and 2010 (Brasil, 2013). The socioeconomic data of the interviewees are summarized in Table 1.

Traditionally, wildlife is valued beyond its economic and simple utilitarian importance when cultural factors associated with their use are considered. On the other hand, there are aspects more directly anthropocentric and utilitarian when birds are recognized as resources to be used for an individual’s own benefit (Costa-Neto, Santos Fita, & Clavijo, 2007). In that sense, social, economic, and cultural factors play an important role in how individuals and communities use those natural resources, leading to a very widely discussed conflict: development versus species preservation (Nobrega et al., 2011).

The Parnaíba Delta has a rich and diversified avifauna, as 97 bird species were cited by the interviewees (individual mean of 8.8 ± 4.87 s.e. [standard error]) from the Labino community in the municipality of Ilha Grande/PI. The birds recognized by the interviewees belonged to 85 genera, 40 families, and 21 orders (Table 2). Although traditional knowledge can often be informative in terms of new species (Cozzuol et al., 2013), all of the species mentioned in the ethno-ornithological survey had been previously recorded in earlier scientific surveys (Guzzi et al., 2015); it is impressive, however, that approximately 60% of the birds recorded in scientific surveys (of a total of 161 species) are recognized on a day-to-day basis by members of the Labino community.

Table 1.
Socio economic profile of community interviewees Labino municipality of Ilha Grande, Piauí State, Brazil.

Table 2
Classification of wild bird species identified as occurring in the community of Labino, rural area of the Municipality of Ilha Grande (Piauí State, Brazil) according to local informants. Birds used as food a; Bird populations reduced over the years d.

Passeriformes were the best represented among the species reported by the interviewees, comprising 29% (n = 28 species) of the total number of species cited, followed by the orders Pelecaniformes, Charadriiformes, and Columbiformes (8%; n = 8 species each); Gruiformes, Cuculiformes, and Piciformes (5%; n = 5 species each). This expressive total of Passeriformes may reflect a preference of the interviewees for singing birds, principally the families Icteridae and Turdidae (species kept as pets), and the Tyrannidae, as well as the abundance of species within that family.

The order Passeriformes consistently shows the greatest species richness in ethno-ornithological studies of the uses and commercialization of birds (Barbosa, Silva, Medeiros, & Chaves, 2014; Galvagne-Loss, Costa-Neto, & Flores, 2014). This order includes birds that are appreciated for their singing and plumage in practically all areas of the tropics, and it is also the most representative order among neotropical birds, with 5,739 known species (Silvius, Bodmer, & Fragoso, 2004) – which helps explain their frequent citations by the interviewees from the Labino community. Columbiformes represent important food resources throughout South America, and species of this order are generally well-known by local human inhabitants (Souza & Alves, 2014). The Columbiformes are important targets for local hunters in northeastern Brazil, and all of its species are killed, captured, and illegally sold for their bush meat. Species of the orders Pelecaniformes and Gruiformes include large birds and those with significant diurnal activities in aquatic environments, which facilitates their observation and recognition by humans (Alves et al., 2012; Souza & Alves, 2014).

The most representative families were Columbidae and Traupidae (8 species each); followed by Ardeidae and Icteridae (6 species); Cuculidade and Picidae (5 species); Rallidae, Scolopacidae, and Psittacidae (4 species). The species with the largest numbers of citations were Columbina picui (n = 109; 73%), Pitangus sulphuratus (n = 97; 65%), Turdus rufiventris, Icterus jamacaii (ambas, n = 71; 47%), Bubulcus ibis and Coragyps atratus (n = 55; 37% each), and Passer domesticus (n = 54; 36%).

Some of the families mentioned as having high species richness in the present study were likewise well-represented in other ornithological surveys in the Parnaíba Delta region (Guzzi et al., 2012, 2015), principally the families Scolopacidae, Ardeidae, and Icteridae in terms of species richness.

Although the richness curve of known species (S(est)) is asymptotic, it is only slightly inclined, and shows a tendency towards stabilization (Figure 2). We were apparently able to record essentially the entire inventory of birds known to the local residents, as Chao2 estimated a richness of approximately 104 species (s.e.= ±5.36 spp.) and second-order Jackknife (Jack2) estimated approximately 114 species (s.e. = 0). The curves of both estimators achieved asymptote with 86 interviewees (Jack2) and 104 interviewees (Chao2) (Figure 2). Consequently, the species inventory demonstrated a sampling effort of 92.3% (comparing S(est) with Chao2) or 84.21% (comparing S(est) with Jack2).

Figure 2.
Accumulation curve of known species mentioned (S (est)) and expected to be known (Chao2 and Jackknife2).

Men recognize more local bird species than women (mean per man = 9.76 ± 5.11; mean per woman = 7.57 ± 4.37; median per man = 9, median per woman = 6). These differences were significant (Mann-Whitney U = 3,613.5; d.f. = 1; p = 0.002; mean ranking (men = 86.05; women = 64.67) (Figure 3A).

The fact that men recognized more bird species than women was not surprising, as hunting activities that involve birds are more frequently or exclusively undertaken by men throughout the tropics, increasing the chances of males utilizing or being aware of more kinetic resources and the ethnoecological aspects of bird species (Alves et al., 2012; Van Vliet et al., 2014). A study undertaken in Pernambuco State (NE Brazil) demonstrated that men retain greater local knowledge about shorebirds and migratory birds than women, which may be related to greater male participation in fishing activities undertaken near avifauna feeding and resting areas (Andrade, Silva-Andrade, Lyra-Neves, Albuquerque, & Telino-Júnior, 2016).

Transgenerational diffusion of ethnozoological knowledge has been cited by a number of authors (Alves & Souto, 2015; Fita, Neto, & Schiavetti, 2010; Souto, Barboza, Rocha, Alves, & Mourão, 2012). We indirectly identified this phenomenon in relation to local ethno-ornithological knowledge, as older individuals generally recognized more bird species than younger members of the community, although this correlation was quite weak (Pearson correlation = 0.164; p = 0.05) (Figure 3B).

The greater levels of knowledge of older individuals corroborated earlier studies focusing on the capture and commercial uses of the tropical fauna (Lindsey et al., 2013; Pangau-Adam, Noske, & Muehlenberg, 2012; Souza & Alves, 2014), suggesting that local knowledge concerning the native fauna is directly influenced by a synergy of factors, including, principally, knowledge transmitted from older individuals to younger relatives, as well as the involvement of a given person in activities that favor frequent contacts with the regional fauna (as, for example, agriculture, land clearing, hunting, and the commercialization of animal products).

Figure 3.
Influence of social aspects on the knowledge of species richness. In 3A, 3C and 3D the dashed line is the median of species richness reported by the entire sample set. In 3B the dashed line is the equation line of the relationship between age and the knowledge of local fauna species. Points external to boxplots in 3A, 3C and 3D represent extreme values (outliers), although they did not significantly alter the median.

Educational levels likewise influences local knowledge about birds (Kruskal-Wallis H = 14.21; d.f. = 2; p < 0.001) (Figure 3C). This difference was observed between individuals with low levels of schooling (illiterate individuals or those that did not finish grammar school) and community members with more education (middle schooling completed or higher) (Dunn post-hoc test, p < 0.05) – with individuals with less schooling demonstrating greater knowledge of species richness than those with more formal educations (Mean ranking low schooling = 88.32, and median = 10; Mean ranking higher education = 58.5, and median = 6). These results demonstrate that a low level of formal schooling do not necessarily imply a poor knowledge of species of the local fauna; these results were similar to those found while studying reproductive aspects of the Psittacidae (Saiki, Guido, & Cunha, 2009) and the ecology of the mangrove crab Ucides cordatus (Cortês, Zappes, & Di Beneditto, 2014) – and may reflect teaching/learning processes – as most school books stress exotic faunas, and more applied students may have less contact with the local avifauna. Time of residence in the community was not found to influence knowledge concerning bird species richness (Kruskal-Wallis H = 7.22; d.f. = 3; p = 0.065) (Figure 3D).

Residents of the Labino community indicated hunting (68%, n=45) as the principle anthropogenic factor impacting the local avifauna. Other factors mentioned were: forest clearing (7% of the respondents), keeping birds as pets (6%), and the illegal commerce in live or dead birds (3%). The predominant perception of hunting as having the greatest impact on the local avifauna is presumably associated with the ample popularity of that activity in northern and northeastern Brazil – areas where birds are frequently converted into bush meat, medicinal products, pets, and adornments (Alves, Lopes, & Alves, 2016; Nascimento, Czaban, & Alves, 2015).

Twenty-three bird species are consumed by the residents of Labino (Table 2), with Aramides cajaneus (Siricora), belonging to the family Rallidae, being the most cited (n=21; 14% of the interviewees), followed by the columbids Columbina squammata (Rolinha-fogo-apagou) (n=19; 13 %) and Zenaida auriculata (Avoante) (n=13; 9%). Columbids, tinamids and birds associated with aquatic environments (e.g., Anseriformes, Gruiformes) were previously identified as preferential hunting targets in different parts of the tropical Americas (Bucher, 1982; Souza & Alves, 2014).

Some bird species can be harvested in large numbers during a single hunting expedition, although they do not present large volumes of meat per individual, nor are they especially appreciated in terms of their flavors, as for example most of the columbids (Bezerra, Araújo, & Alves, 2012; Von Ihering, 1935). Zenaida auriculata, Columbina spp., Anas bahamensis and Aramides cajaneus were frequently mentioned by the interviewees in that context. There was no influence of gender (Mann-Whitney U = 3.074, p > 0.05), age (Pearson correlation, p > 0.05), schooling (Kruskal-Wallis H, p > 0.05), or time of residence (Kruskal-Wallis H, p > 0.05) on the richness of bird species consumed by the interviewees.

A total of 48 bird species were perceived as having their populations reduced in recent years (Table 2). The species most cited in this sense by the interviewees were: Mimus gilvus (Sabiá-da-praia) (n=15), Icterus jamacaii (Corrupião) (n=13), Aramides cajaneus (Siricora) (n=12), Turdus rufiventris (Sabiá-laranjeira) (n=9), Cacicus cela (Xexéu), Pitangus sulphuratus (Bem-te-vi) (n=8), Anas bahamensis (Marreca) (n=6), Columbina picui (Rolinha branca) (n=5), Vanellus chilensis (Quero-quero), and Tangara sayaca (Sanhaçu) (n=4). With the exception of Aramides cajaneus, the diminishing species normally show only low sensitivity to environmental alterations and considerable plasticity in terms of their tolerance of anthropogenic impacts (according to the interviewees) (Silva, Souza, Bieber, & Carlos, 2003).

The species cited as demonstrating population reductions are not considered threatened species (Instituto Chico Mendes de Conservação da Biodiversidade [ICMbio], 2018) by the International Union for the Conservation of Nature (IUCN, 2019), being classified in the “less concern” conservation category (category LC) (IUCN, 2019). The red list, however, considers species populations throughout their entire distribution range, even while some local populations could be depleted or eradicated. Ecological studies of bird populations in the Parnaiba Delta are urgently needed in light of the information provided by local residents.

The socioeconomic aspects of the residents of the Labino community, such as their gender (Mann-Whitney U, p > 0.05), age (Pearson correlation, p > 0.05), levels of schooling (Kruskal-Wallis H, p > 0.05), and time of residents in the community (Kruskal-Wallis H, p > 0.05) were not found to influence their perception of reduced species richness.