Acessibilidade / Reportar erro

Ecology, interactions and human perceptions of Cerdocyon thous in rural landscapes in the state of Pernambuco, Brazil

Abstract

Human populations maintain diverse relationships with wild animals that lead to both positive and negative interactions. The aim of the present study was to investigate the ecology, interactions and human perceptions of Cerdocyon thous in rural landscapes in the state of Pernambuco in northeastern Brazil. Interviews were held from November to December 2015. Data collection involved the use of a semi-structured questionnaire and photographs of the fox. Most interviewees (96.94%) demonstrated knowledge of the species, attributing eight different vernacular denominations to the animal. The interviewees also demonstrated knowledge regarding its habitats, active hours, diet, behavior and diseases. The respondents pointed out negative aspects, such as the transmission of diseases (48.72%), the death of domesticated animals and consequent negative economic impact (42.74%), attacks against humans and other animals (6.84%) and causing an environment imbalance (1.70%). The positive roles attributed to the fox regarded its use as a resource for medicinal purposes, craftwork, mystical-religious ceremonies and as a pet. There is a need for further information on C. thous and adequate protection measures should be taken in local communities to ensure the conservation of the species in rural landscapes.

Key words
Local knowledge; ethnozoology; rural areas; northeastern Brazil; fox

INTRODUCTION

The expansion of livestock farming in northeastern Brazil is reflected in the conversion of forests into pastures and farms. Policies and programs in the region are insufficient and often inconsistent, since they are based on poor knowledge regarding resources and the complexities of the human-environment relationship (Albuquerque & Andrade 2002ALBUQUERQUE UP & ANDRADE LHC. 2002. Uso de recursos vegetais da caatinga: o caso do agreste do estado de Pernambuco (Nordeste do Brasil). Interciencia 27: 336-346.). This region encompasses different landscapes that have been undergoing changes due to human activities since the colonial period.

The Agreste is a transition region between the rainforest zone of the coast and the semi-arid interior of northeastern Brazil that incorporates the Atlantic forest and Caatinga biomes. The Agreste primarily has sugarcane plantations and livestock farming activities, but also has productive diversity due to the variety of microclimates, soils and reliefs, including areas specialized in dairy cattle farming, fruit and vegetable crops, sisal, beef cattle farming and subsistence farming, such as beans, corn and manioc (Mueller 1996MUELLER CC. 1996. Organização e ordenamento do espaço regional do Nordeste. Planejamento e Políticas Públicas, IPEA n.13, p. 35-111.).

The Atlantic Forest biome in northeastern Brazil has pioneering formations, portions of dense and open rainforest, semi-deciduous and deciduous seasonal forests and is home to four of the five centers of endemism of the biome. However, it is the most degraded region, with dozens of officially endangered species (Tabarelli et al. 2006TABARELLI M, MELO MDVC & LIRA OC. 2006. A Mata Atlântica do nordeste. In: Campanili M & Prochnow M (Eds). Mata Atlântica - uma rede pela floresta. RMA, Brasília, p. 1-17.). The Atlantic Forest is highly fragmented, with high rates of reduction, which is the major threat to mammals (Chiarello 1999CHIARELLO AG. 1999. Effects of fragmentation of the Atlantic forest on mammal communities in southeastern Brazil. Biol Conserv 89: 71-82., Onderdonk & Chapman 2000ONDERDONK D & CHAPMAN C. 2000. Coping with forest fragmentation: The primates of Kibale National Park, Uganda. Int J Primatol 21: 587-611., Fahrig 2003FAHRIG L. 2003. Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Evol Syst 34: 487-515.).

In recent decades, the loss of biodiversity around the world has occurred on a scale without precedent and the intensification of agriculture is one of the main reasons for this global change (Matson et al. 1997MATSON PA, PARTON WJ, POWER AG & SWIFT MJ. 1997. Agricultural intensification and ecosystem properties. Science 277: 504-509., Tilman et al. 2001TILMAN D, FARGIONE J, WOLFF B, D’ANTONIO C, DOBSON A, HOWARTH R, SCHINDLER D, SCHLESINGER WH, SIMBERLOFF D & SWACKHAMER D. 2001. Forecasting agriculturally driven global environmental change. Science 292: 281-284.). Many carnivorous mammals are currently in a vulnerable or even critical state in terms of conservation and the major cause of the decline in the populations of these animals is the reduction or loss of habitats due to the expansion of agriculture, livestock farming and human colonization (Santos et al. 2004SANTOS MFM, PELLANDA M, TOMAZZONI AC, HASENACK H & HARTZ SM. 2004. Mamíferos carnívoros e sua relação com a diversidade de hábitats no Parque Nacional dos Aparados da Serra, sul do Brasil. Iheringia Sér Zool 94: 235-245.).

Conflicts between humans and carnivores constitute an urgent challenge to the conservation of these animals, especially on the recent frontiers of deforestation and rural landscapes, where the requirements of the living area and diet of carnivores are often in discord with human activities (Michalski et al. 2006MICHALSKI F, BOULHOSA RLP, FARIA A & PERES CA. 2006. Human–wildlife conflicts in a fragmented Amazonian forest landscape: determinants of large felid depredation on livestock. Anim Conserv 9: 179-188.). Therefore, designing effective strategies for the conservation of native species in landscapes that have been modified by humans requires an understanding of how wild species use these spaces (Ferreira et al. 2018FERREIRA AS, PERES CA, BOGONI JÁ & CASSANO CR. 2018. Use of agroecosystem matrix habitats by mammalian carnivores (Carnivora): a global-scale analysis. Mamm Rev 48: 312-327.).

Although the threats of habitat loss and fragmentation are serious, another important cause of death of adult carnivores is the hostility of humans (Woodroffe & Ginsberg 1998WOODROFFE R & GINSBERG JR. 1998. Edge effects and the extinction of populations inside protected areas. Science 280: 2126-2128.). A large number of carnivorous species are vulnerable to hunting, slaughter, poisoning, accidental deaths, being run over by a vehicle and other sources of death (Michalski et al. 2006MICHALSKI F, BOULHOSA RLP, FARIA A & PERES CA. 2006. Human–wildlife conflicts in a fragmented Amazonian forest landscape: determinants of large felid depredation on livestock. Anim Conserv 9: 179-188.).

The diverse interactions between humans and wild animals enable individuals to perceive and interpret the world they know in their own way (Gibson 1979GIBSON JJ. 1979. The Ecological Approach to Visual Perception. Boston: Houghton Mifflin, Boston, 332 p., Pezzuti & Chaves 2009PEZZUTI J & CHAVES RP. 2009. Etnografia e manejo de recursos naturais pelos índios Deni, Amazonas, Brasil. Acta Amaz 39: 121-138.). Wildlife directly and indirectly contributes to the subsistence of human communities and has been used as source of food, medicine, trade, ornamentation, recreation, ceremony and companionship (Alves & Souto 2010ALVES RRN & SOUTO WMS. 2010. Etnozoologia: conceitos, considerações e importância. In: Alves RRN et al. (Eds), Etnozoologia no Brasil: importância, status atual e perspectivas. NUPEEA. Recife, p. 21-40.). However, there are also conflictive aspects of these relationships due to aggressive behavior, as some animals may attack other animals and people and some human cultural activities, such as hunting, target these animals. Carnivores are the mammals most involved in conflicts with humans, as some species are tracked and killed due to risks associated with the transmission of disease, harm to farming activities and the predation of domestic animals (Alves et al. 2009ALVES RRN, MENDONÇA LET, CONFESSOR MVA, VIEIRA WLS & LOPES LCS. 2009. Hunting strategies used in the semi-arid region of northeastern Brazil. J Ethnobiol Ethnomed 5: 1-16., Mendonça et al. 2011MENDONÇA LET, SOUTO CM, ANDRELINO LL, SOUTO WMS, VIEIRA WLS & ALVES RRN. 2011. Conflitos entre pessoas e animais silvestres no Semiárido paraibano e suas implicações para conservação. Sitientibus Ser Cienc Biol 11: 185-199.). Such conflicts have been recorded ever since animals were first domesticated (Nowell & Jackson 1996NOWELL K & JACKSON P. 1996. Wild Cats. Status Survey and Conservation Action Plan. IUCN/SSC Cat Specialist Group, Gland, Switzerland.) and result from the sharing of the same habitats and resources (García-Grajales 2013GARCÍA-GRAJALES J. 2013. El conflicto hombre-cocodrilo en México: causas e implicaciones. Interciencia 38: 881-884.).

Cerdocyon thous (Linnaeus, 1766) is a medium-sized carnivorous canine knowned as crab-eating fox, forest fox, wood fox or Maikong with distribution from northern South America and south of Amazonia to northern Argentina (Courtenay & Maffei 2004COURTENAY O & MAFFEI L. 2004. Crab-eating Fox Cerdocyon thous. In: Sillero-Zubiri C et al. Canids: foxes, wolves, jackals and dogs. Status survey and conservation action plan, IUCN / SSC Canid Specialist Group, IUCN, Gland, Switzerland and Cambridge, UK, p. 32-38.. In Brazil, this fox is found in all biomes (Beiseigel et al. 2013BEISEIGEL BM, LEMOS FG, AZEVEDO FC, QUEIROLO D & JORGE RS. 2013. Avaliação do risco de extinção do cachorro-do-mato Cerdocyon thous (Linnaeus, 1766) no Brasil. Instituto Chico Mendes de Conservação da Biodiversidade, p. 138-143.), inhabiting modified landscapes, sugarcane plantations and areas near roads and highways.

Although C. thous has a broad distribution, there are gaps in knowledge regarding its use of habitat, biology and conflicts with humans on agricultural lands. Thus, the aim of the present study was to investigate the ecology, interactions and human perceptions of Cerdocyon thous in rural landscapes in the Agreste and coastal forest zone of the state of Pernambuco in northeastern Brazil.

MATERIALS AND METHODS

Study area

The survey was conducted in 36 rural locations in four municipalities in the state of Pernambuco: one in the Agreste - Feira Nova (07° 57’03” S and 35° 23’21” W); area: 107,726 km²; number of inhabitants: 20.571 and three in the coastal forest zone - Glória do Goitá (08° 00’06” S and 35° 17’34” W); area: 231,832 km²; number of inhabitants: 29.019; Paudalho (07° 53 48” S and 35° 10’47” W); area: 274,776 km²; number of inhabitants: 51.357; and Vitória de Santo Antão (08° 07’05” S and 35° 17’29” W); area: 335,941 km²; number of inhabitants: 129.974 (CPRM 2005CPRM. 2005. Serviço geológico do Brasil. Mapa geológico do Estado de Pernambuco. Ministério de Minas e Energia- Secretária de Mineração e transformação mineral. Brasília. Disponível em: < http://www.cprm.gov.br>. Acesso em 22 de junho de 2018.
http://www.cprm.gov.br...
, IBGE 2018IBGE - INSTITUTO BRASILEIRO DE GEOGRAFIA E ESTATÍSTICA. 2018. Censo Populacional 2010. Disponível em: <https://cidades.ibge.gov.br/brasil/pe/panorama> último acesso 18 de julho de 2018.
https://cidades.ibge.gov.br/brasil/pe/pa...
) (Figure 1). Vitória de Santo Antão has the largest area and number of inhabitants in both the urban (113.429) and rural (16.545) zones. Feira Nova has the smallest rural area and smallest number of inhabitants in the rural zone (4.258). Glória do Goitá has the smallest number of inhabitants in the urban zone (15.434) (IBGE 2018IBGE - INSTITUTO BRASILEIRO DE GEOGRAFIA E ESTATÍSTICA. 2018. Censo Populacional 2010. Disponível em: <https://cidades.ibge.gov.br/brasil/pe/panorama> último acesso 18 de julho de 2018.
https://cidades.ibge.gov.br/brasil/pe/pa...
).

Figure 1
Map of Pernambuco highlighting municipalities of Feira Nova, Paudalho, Glória de Goitá and Vitória de Santo Antão.

The climate is characterized as rainy tropical, with the rainy season (peak between June and July) and a dry season with a mean temperature of 30.5 °C (INMET 2015INMET - INSTITUTO NACIONAL DE METEOROLOGIA. 2015. Disponível em: <www.inmet.gov.br/portal/index.php?r=home2/pageepage>. Disponível em 06 de abril de 2015.
www.inmet.gov.br/portal/index.php?r=home...
). The main vegetal formations are semi-deciduous forests with trees reaching 20 m, semi-evergreen forests, quite devastated deciduous forests with trees reaching 10 m and hypoxerophilic Caatinga (dry scrubland) (CPRM 2005CPRM. 2005. Serviço geológico do Brasil. Mapa geológico do Estado de Pernambuco. Ministério de Minas e Energia- Secretária de Mineração e transformação mineral. Brasília. Disponível em: < http://www.cprm.gov.br>. Acesso em 22 de junho de 2018.
http://www.cprm.gov.br...
).

The municipalities are characterized by a predominance of rural properties, with a rural economy focused on craftwork, small livestock farming and agriculture, predominantly subsistence farming as well as cassava, fruit, vegetable crops and sugarcane plantations.

Procedures

Interviews with residents of rural areas were conduced in November and December 2015. We first showed a photograph of C. thous to see if the interviewees identified the species and we commented on aspects of its biology, morphology and ecology. Subsequently, semi-structured questionnaires were applied based on Bernard (Bernard 1994BERNARD HR. 1994. Research Methods in: Anthropology: Qualitative and Quantitative Approaches. Sage. Thousand Oaks, CA, EEUU, p. 824.). The data were analyzed using the “union of diverse individual skills” model (Marques 2001MARQUES JGW. 2001. Pescando pescadores: Ciência e Etnociência em uma Perspectiva Ecológica. NUPAUB, USP. São Paulo, Brasil, p. 258.). Whenever possible, descriptive statistics were performed (mean, standard deviation and relative frequency). This study received approval from the Human Research Ethics Committee of the Center for Health Sciences of the Federal University of Pernambuco (certificate number: 49839915.7.0000.5208).

RESULTS AND DISCUSSION

Socioeconomic aspects of respondents

One hundred ninety-eight individuals were interviewed: 113 (57.07%) men and 85 (42.93%) women with ages ranging from 19 to 80 years (mean: 53.89 ± 13.88 years). Mean age was 51.71 ± 14.16 years among the men and 56.8 ± 11.66 years among the women. The socioeconomic data of the respondents are summarized in Table I.

Table I
Socioeconomic aspects of respondents in study areas in Agreste and coastal forest zone of state of Pernambuco, Brazil (N; %).

Ecology of C. thous in agricultural landscapes

Natural areas and locations altered by human activities were cited as the habitat of C. thous, which is in agreement with data described in the literature. According to Lemos et al. (2011a)LEMOS FG, AZEVEDO FC, COSTA HCM & JUNIOR JAM. 2011b. Human threats to hoary and crab-eating foxes in central Brazil. Canid News 14: 1-6., this fox is tolerant to anthropogenic disturbance and altered landscapes; moreover, the occurrence of this canine in various environments is related to different levels of disturbance. Dias et al. (2014)DIAS DM, RIBEIRO AS, BOCCHIGLIERI A & PEREIRA TC. 2014. Diversidade de carnívoros (mammalia: carnivora) da serra dos macacos, Tobias Barreto, Sergipe. Biosci J 30: 1192-1204. report that it is common for this animal to use the interior and edges of forests. Courtenay & Maffei (2004) report that the species inhabits altered areas near habitations. Juarez & Marinho-Filho (2002)JUAREZ KM & MARINHO-FILHO J. 2002. Diet, habitat use, and home ranges of sympatric canids in Central Brazil. J Mammal 83: 925-933. recorded the species in farming areas. In the present study, C. thous was reported in different habitats, especially woodlands (47.61%) among natural environments and sugarcane plantations (16.34%) among areas transformed by human activities (Figure 2). Although there is also evidence of carnivores that adapt to a wide variety of habitats impacted by humans, it is important identify the limits of their tolerance and their preferences, which can only be investigated in areas of greater interface with humans (Athreya et al. 2013ATHREYA V, ODDEN M, LINNELL JDC, KRISHNASWAMY J & KARANTH U. 2013. Big Cats in Our Backyards: Persistence of Large Carnivores in a Human Dominated Landscape in India. PLoS ONE 8: e57872.). This adaptation demonstrates the high ecological plasticity of C. thous, which is evidenced in areas near plantations, residences and roadways, despite its preference for natural environments in the present study.

Figure 2
Environments related to the presence of C. thous cited by respondents.

A total of 42.86% of the interviewees reported that C. thous was more active at night, 34.36% cited the morning hours, 22.39% cited the afternoon hours and 0.39% cited the predawn hours. Indeed, the species has nocturnal and twilight habits, traveling alone or in pairs along the edges of forests and roads (Rocha et al. 2004ROCHA VJ, REIS NR & SEKIAMA ML. 2004. Dieta e dispersão de sementes por Cerdocyon thous (Linnaeus) (Carnívora, Canidae), em um fragmento florestal no Paraná, Brasil. Rev Bras Zool 21: 871-876., Reis et al. 2006REIS NR, PERACCHI AL, PEDRO WA & LIMA IP. 2006. Mamíferos do Brasil. Londrina, p. 437., Abreu Júnior & Kohler 2009ABREU JÚNIOR EF & KOHLER A. 2009. Mastofauna de médio e grande porte na RPPN da UNISC. Biota Neotrop 9: 169-174.), where the animals are easily sighted searching for food. Some authors state that the period of activity is related to the period of activity of its prey items (Maffei & Taber 2003MAFFEI L & TABER AB. 2003. Área de acción, actividad y uso de hábitat del zorro patas negras, Cerdocyon thous, en un bosque seco. Mastozool Neotrop 10: 154-160.). According to Beltrán & Delibes (1994)BELTRÁN J & DELIBES M. 1994. Environmental determinants of circadian activity o free-ranging Iberian lynxes. J Mammal 75: 382-393., environmental factors can exert an influence on the period of activity of the crab-eating fox. Activity in the morning and afternoon may be a reflection of the environmental change of the rural landscape, which may lead to an increase in encounters with humans.

Different food items consumed by the crab-eating fox were cited. The most frequently cited group was birds (77.20%), represented mainly by chickens (Table II). C. thous is considered a generalist species. Rocha et al. (2004)ROCHA VJ, REIS NR & SEKIAMA ML. 2004. Dieta e dispersão de sementes por Cerdocyon thous (Linnaeus) (Carnívora, Canidae), em um fragmento florestal no Paraná, Brasil. Rev Bras Zool 21: 871-876. report that vertebrates are the most consumed food items by the species, especially rodents and birds, as well as reptiles, small invertebrates (insects) and a large number of vegetal items, including leaves and grasses. According to Chieregatto et al. (2003)CHIEREGATTO A, CALZOLARI F, TRASFORINI G, TARGA L & LATRONICO N. 2003. Normal jugular bulb oxygen saturation. J Neurol Neurosur Ps 74: 784-786., this canine feeds on insects, vertebrates, invertebrates and fruits, but has a preference for rodents and has a seasonal diet that varies according to the most abundant resources in the rainy and dry seasons. The effects of an agricultural environment altered by human activities include the presence of non-native rodents and C. thous plays an important role in controlling such populations (Rocha et al. 2004ROCHA VJ, REIS NR & SEKIAMA ML. 2004. Dieta e dispersão de sementes por Cerdocyon thous (Linnaeus) (Carnívora, Canidae), em um fragmento florestal no Paraná, Brasil. Rev Bras Zool 21: 871-876., Kasper et al. 2007KASPER CB, FELDENS MJ, MAZIM FD, SCHNEIDER A, CADEMARTORI CV & GRILLO HCZ. 2007. Mamíferos do Vale do Taquari, Região Central do Rio Grande do Sul. Biocienc 15: 53-62.).

Table II
Food items consumed by crab-eating fox mentioned by respondents.

Mendonça et al. (2011)MENDONÇA LET, SOUTO CM, ANDRELINO LL, SOUTO WMS, VIEIRA WLS & ALVES RRN. 2011. Conflitos entre pessoas e animais silvestres no Semiárido paraibano e suas implicações para conservação. Sitientibus Ser Cienc Biol 11: 185-199. report that these foxes often attack small farm animals due to habitat fragmentation and the reduction in the number of natural preys. In the present study, the generalist habit the crab-eating fox was confirmed and a preference for birds, especially chickens, was reported due to the abundance of this group on small farms in the region, demonstrating the adaptability of C. thous to rural landscapes for the purposes of survival.

The majority of interviewees (86.15%) reported that C. thous demonstrates aggressive behavior during the reproductive period or after having given birth, whereas 12.82% reported that the animal is not aggressive and 1.03% were uncertain. According to the interviewees, the reproductive period may be influenced by the phases of the new and full moon and occurs in both winter and summer. Mendonça et al. (2011)MENDONÇA LET, SOUTO CM, ANDRELINO LL, SOUTO WMS, VIEIRA WLS & ALVES RRN. 2011. Conflitos entre pessoas e animais silvestres no Semiárido paraibano e suas implicações para conservação. Sitientibus Ser Cienc Biol 11: 185-199. also recorded interviewees in the semiarid region of the state of Paraíba who stated that the crab-eating fox is aggressive after having given birth to a litter and, according to hunters in the region, the species is considered dangerous and aggressive, with the possibility of attacking humans.

Human perceptions

The vast majority of interviewees (96.94%) was able to identify the species, which may be explained by the fact that it is a common canine that is easily encountered in diverse environments and is broadly distributed throughout Brazil (Beiseigel et al. 2013BEISEIGEL BM, LEMOS FG, AZEVEDO FC, QUEIROLO D & JORGE RS. 2013. Avaliação do risco de extinção do cachorro-do-mato Cerdocyon thous (Linnaeus, 1766) no Brasil. Instituto Chico Mendes de Conservação da Biodiversidade, p. 138-143.), including the entire state of Pernambuco as well as areas heavily altered by human activities (Cruz et al. 2002CRUZ MAOM, BORGES-NOJOSA DM, LANGGUTH AR, SOUZA MAN, SILVA LAM, LEITE LMRM, PRADO FMV, VERÍSSIMO KCS & MORAES BLC. 2002. Diversidade de mamíferos em áreas prioritárias para conservação da caatinga, p. 182-226.). In a study conducted in the semiarid region of the northeastern Brazil, Dias et al. (2014)DIAS DM, RIBEIRO AS, BOCCHIGLIERI A & PEREIRA TC. 2014. Diversidade de carnívoros (mammalia: carnivora) da serra dos macacos, Tobias Barreto, Sergipe. Biosci J 30: 1192-1204. report that recognizing and interacting with native species is a common occurrence in many locations. Mendonça et al. (2011)MENDONÇA LET, SOUTO CM, ANDRELINO LL, SOUTO WMS, VIEIRA WLS & ALVES RRN. 2011. Conflitos entre pessoas e animais silvestres no Semiárido paraibano e suas implicações para conservação. Sitientibus Ser Cienc Biol 11: 185-199. found that farmers in the state of Paraíba have knowledge on local species, including carnivores. In a study conducted in the municipality of Lapão in the state of Bahia, Barbosa et al. (2014)BARBOSA A, OLIVEIRA DSC & OLIVEIRA CRM. 2014. Uso tradicional da fauna silvestre do município de Lapão Bahia. Enciclopédia Biosfera 10: 118-133. found that the majority of local residents have knowledge on wildlife in the region, including C. thous.

The species received different denominations from the interviewees, such as cat fox (36.73%), dog fox (36.42%), fox (11.73%), forest dog (4.94%), forest cat (4.32%), forest fox (4.01%), guará (1.23%) and wolf (0.62%). According to Cruz et al. (2002)CRUZ MAOM, BORGES-NOJOSA DM, LANGGUTH AR, SOUZA MAN, SILVA LAM, LEITE LMRM, PRADO FMV, VERÍSSIMO KCS & MORAES BLC. 2002. Diversidade de mamíferos em áreas prioritárias para conservação da caatinga, p. 182-226., the species is also known as goró, mariano and guaspira in the state of Pernambuco.

Among the interviewees, 53.53% had not had any contact with the animal, whereas 26.77% had any direct physical contact, such as a touch and bites and 19.70% only observed the foxes in the proximities of residences, roads, woods, sugarcane plantations, roadways and farms.

The majority of interviewees (53.46%) stated that the animal has no importance, 23.90% did not know whether the animal has importance and 22.64% stated that the crab-eating fox does indeed have importance.

Among the group who reported that C. thous has importance, 68.63% cited positive aspects and 31.37% cited negative aspects. The positive aspects were categorized in forms of use: craftwork, medicinal, mystical-religious activities and companionship (Table III). According to Marques (2001)MARQUES JGW. 2001. Pescando pescadores: Ciência e Etnociência em uma Perspectiva Ecológica. NUPAUB, USP. São Paulo, Brasil, p. 258., human populations attribute importance to the species they know better and for which they have feelings and beliefs. In a study on the knowledge and use of fauna by hunters in the semiarid region of the state of Paraíba, Barbosa & Aguiar (2015)BARBOSA JAA & AGUIAR JO. 2015. Conhecimento e usos da fauna por caçadores no semiárido brasileiro: Um estudo de caso no estado da Paraíba, Nordeste do Brasil. Biotemas 28: 137-148. recorded different forms of use, such as medicinal (treatment of ailments), mystical-religious (inclusion of animals in rituals), as pets and as a food source. In another study conducted in the semiarid region of northeastern Brazil, Barbosa & Aguiar (2012)BARBOSA JAA & AGUIAR JO. 2012. Utilização místico-tradicional da fauna no semiárido paraibano, Paraíba, Brasil. Polêm!ca 11: 642-649. report that different species of fauna are used for mystical-religious purposes, such as amulets for the “evil-eye”, sacrificial rituals, cures for spiritual illnesses and folk stories. With regard to negative aspects, C. thous was seen as a species that causes conflicts due to the predation of farm animals and the transmission of disease, giving it a poor image in the communities surveyed.

Table III
Forms of use of C. thous identified by the communities studied (Agreste and coastal forest zone of state of Pernambuco, Brazil).

Understanding the relationships that have been established between humans and animals is an important step in ensuring the sustainable use of the local/regional fauna and avoiding conflicts with communities (Licarião et al. 2013LICARIÃO MR, BEZERRA DMM & ALVES RRN. 2013. Wild birds as pets in Campina Grande, Paraíba State, Brazil: An Ethnozoological Approach. An Acad Bras Cienc 85: 201-213.). Wild animals have been kept as companions for centuries and this widely spread traditional practice involves hundreds of species (Alves et al. 2013ALVES RRN, LIMA JRF & ARAÚJO HF. 2013. The live bird trade in Brazil and its conservation implications: an overview. Bird Conserv Int 23: 53-65.). In the present study, some interviewees reported that C. thous can serve a pet if raised from a very young age (Table III). In a study conducted with residents of the semiarid region of northeastern Brazil, Alves et al. (2016)ALVES MM, LOPES SF & ALVES RRN. 2016. Wild Vertebrates kept as pets in the semiarid region of Brasil. Trop Conserv Sci 9: 354-368. report the occurrence of keeping wild animals as pets, which are often consumed as a food source by the “owners”. The earliest archaeological records from South America clearly indicate that although endemic foxes may never have been fully domesticated at any time, it is entirely conceivable that in the absence of the domesticated Canis familiaris, humans may have developed some sort of symbiotic relationship with foxes (Stahl 2012STAHL PW. 2012. Interactions between humans and endemic canids in Holocene South America. J Ethnobiol 32: 108-127.). However, Brazilian legislation prohibits the use of wild animals as pets or as a source of food. Transgressors can be subject to punishment and the practice exerts a negative impact on the conservation of C. thous. From the conservationist standpoint, it is preferable to keep domesticated animals, such as dogs, cats, chickens, etc. (Alves et al. 2013ALVES RRN, LIMA JRF & ARAÚJO HF. 2013. The live bird trade in Brazil and its conservation implications: an overview. Bird Conserv Int 23: 53-65.), so that fewer wild animals are removed from their natural environment, diminishing the fragmentation and degradation of habitats and reducing conflicts between these animals and human beings.

Conflicts associated with the species

According to a global-scale review performed by Ferreira et al. (2018)FERREIRA AS, PERES CA, BOGONI JÁ & CASSANO CR. 2018. Use of agroecosystem matrix habitats by mammalian carnivores (Carnivora): a global-scale analysis. Mamm Rev 48: 312-327., only 7% of all studies report that the use of agroecosystems by carnivores resulted in conflicts with local human livelihoods, such as crop raiding, crop damage, livestock depredation and lethal or non-lethal injury to local people. In the study area, a total of 52.53% of the interviewees stated that C. thous causes problems for humans, whereas 32.32% stated that the animal does not cause problems and 15.15% were reported not knowing. The most cited problems were the transmission of diseases (48.72%), the death of domesticated animals and consequent negative economic impact (42.74%), attacks against humans and other animals (6.84%) and causing an environment imbalance (1.70%), with negative impacts on the communities. In the study by Mendonça et al. (2011)MENDONÇA LET, SOUTO CM, ANDRELINO LL, SOUTO WMS, VIEIRA WLS & ALVES RRN. 2011. Conflitos entre pessoas e animais silvestres no Semiárido paraibano e suas implicações para conservação. Sitientibus Ser Cienc Biol 11: 185-199., residents of the semi-arid region in the state of Paraíba reported that foxes cause damage to crops, attack domesticated animals and transmit diseases to the residents.

Six types of diseases were associated with the crab-eating fox, which were categorized as respiratory problems (shortness of breath, asthma and allergies), skin disease (mange, rash, itching and dermatosis), phobias and fear, infections, leishmaniasis and rabies, the latter of which was the most cited (Figure 3).

Figure 3
Diseases cited by interviewees related to crab-eating fox.

Wild canids corresponded to 88% of rabies cases reported in the northeastern Brazil from 2002 to 2009 (Wada et al. 2011WADA MY, ROCHA SM & MAIA-ELKHOURY ANS. 2011. Situação da raiva no Brasil, 2000 a 2009. Epidemiol Serv Saúde 20: 509-518.). According to Kotait et al. (2007)KOTAIT I, CARRIERI ML, CARNIELI JRP, CASTILHO JG, OLIVEIRA RN, MACEDO CI, FERREIRA KCS & ACHKAR SM. 2007. Reservatórios silvestres do vírus da raiva: um desafio para a saúde pública. BEPA, Bol Epidemiol Paul 4: 02-08., foxes in northeastern Brazil serve as reservoirs for rabies, with reports of transmission to humans (Bernardi et al. 2005BERNARDI F, NADIN-DAVIS SA, WANDELER AI, ARMSTRONG J, GOMES AAB, LIMA FS, NOGUEIRA FR & ITO FH. 2005. Antigenic and genetic characteization of rabies viroses isolated from domestic and wild animals of Brazil identifies the hoary fox as a rabies reservoir, J Gen Virol 86: 3153-3162.). Moreover, Jorge et al. (2010)JORGE RSP, ROCHA FL, MAY JA & MORATO RG. 2010. Ocorrência de patógenos em carnívoros selvagens brasileiros e suas implicações para a conservação e saúde pública. Oecol Aust 14: 686-710. report the exposure of C. thous to distemper, Leishmania spp and parvovirus. For northeastern Brazil, Cerqueira et al. (1998)CERQUEIRA EJL, SILVA EM, MONTE-ALEGRE AF & SHERLOCK IA. 1998. Considerações sobre pulgas (Siphonaptera) da raposa Cerdocyon thous (Canidae) da área endêmica de leishmaniose visceral de Jacobina, Bahia, Brasil. Rev Soc Bras Med Tro 33: 91-93. report that C. thous is the only species of fox infected by Leishmania chagasi.

In a study conducted with residents of the semiarid region of the state of Paraíba, Mendonça et al. (2011)MENDONÇA LET, SOUTO CM, ANDRELINO LL, SOUTO WMS, VIEIRA WLS & ALVES RRN. 2011. Conflitos entre pessoas e animais silvestres no Semiárido paraibano e suas implicações para conservação. Sitientibus Ser Cienc Biol 11: 185-199. report that the risk of the transmission of diseases by C. thous is related to the destruction of natural habitats due to farming and livestock activities as well as the accumulation of trash, which attracts these animals to human settlements. According to Alexander et al. (2002)ALEXANDER B, CARVALHO RL, CALLUM MCH & PEREIRA MH. 2002. Roler of the domestic chicken (Gallus gallus) in the epidemiology of urban visceral leishmaiasis in Brasil. Emerg Infect Dis 8: 1480-1485., such contact further increases the participation of the crab-eating fox in the transmission of diseases. In a study conducted in the state of Sergipe by Antunes et al. (2018)ANTUNES KD ET AL. 2018. Descriptive analysis of rabies in wild animals in the state of Sergipe, Brazil. Arq Bras Med Vet Zootec 70: 169-173., the rabies virus circulates opening in the wild, leading to the spread of the disease to urban and rural environments. This situation imposes the need for a permanent, systematic epidemiological surveillance of rabies among key wild species, such as primates, bats and carnivores, in natural environments. In the present study, the crab-eating fox was commonly sighted in the areas surroundings agricultural activities for the raising of domesticated animals, especially birds, which explains the negative view that the interviewees had regarding the species, as such contact very often results in the predation of small farm animals besides the transmission of diseases.

In the reports of 7.77% of the interviewees, aggression toward domesticated dogs (C. familiaris) by the crab-eating fox caused conflictive relations that resulted in the death of foxes. According to Beisiegel et al. (2013), conflicts between dogs and C. thous are common, especially when the fox approaches homes in search of food. Lemos et al. (2011b)LEMOS FG, FACURE KG & AZEVEDO FCA. 2011a. First approach to the comparative ecology of the hoary fox and the crab-eating fox in a fragmeted human altered landscape in the Cerrado biome at central Brasil. In: Rosalino LM & Costa-Gheler C. Middle-sized carnivores in agricultural landscapes. Nova Science Publishers, New York, p. 143-160. report aggression and the death of foxes by dogs on cattle farms in the state of Goiás and on a federal road in the state of Minas Gerais. A study conducted in India reports that domesticated dogs exert a negative impact on thespatial distribution of the fox Vulpes bengalensis and are an important cause of the mortality of the species (Vanak & Gompper 2010VANAK AT & GOMPPER ME. 2010. Interference competition at the landscape level: the effect of free-ranging dogs on a native mesocarnivore. J Appl Ecol 47: 1225-1232.).

When asked what should be done in cases of a domesticated animal being attacked, 55.17% stated that the animal should be vaccinated, 20.69% would seek a veterinarian, 6.90% would sacrifice the animal and 17.24% did not know what should be done. With regard to attacks against humans, 67.07% stated that the proper course of action would be a rabies vaccine, 22.16% state that they would seek a healthcare service, 5.99% did not know what should be done, 3.59% reported they would take medication and 1.20% would wash the bite wound. Although the majority of interviewees demonstrated knowledge on what should be done following aggression or an attack by C. thous, there is a need for prevention and control measures for this zoonosis in rural areas.

Attacks by crab-eating foxes should be carefully verified, as this animal is one of the main reservoirs of wild rabies (Kotait et al. 2007KOTAIT I, CARRIERI ML, CARNIELI JRP, CASTILHO JG, OLIVEIRA RN, MACEDO CI, FERREIRA KCS & ACHKAR SM. 2007. Reservatórios silvestres do vírus da raiva: um desafio para a saúde pública. BEPA, Bol Epidemiol Paul 4: 02-08.) and the fact that it lives in areas near human activities increases the odds of contact with humans and the possible transmission of this disease. The prevention of attack, together with vaccination programs and the birth control of domesticated dogs could potentially reduce the rate of contact between dogs and wild carnivores (Vanak & Gompper 2010VANAK AT & GOMPPER ME. 2010. Interference competition at the landscape level: the effect of free-ranging dogs on a native mesocarnivore. J Appl Ecol 47: 1225-1232., Lemos et al. 2011bLEMOS FG, FACURE KG & AZEVEDO FCA. 2011a. First approach to the comparative ecology of the hoary fox and the crab-eating fox in a fragmeted human altered landscape in the Cerrado biome at central Brasil. In: Rosalino LM & Costa-Gheler C. Middle-sized carnivores in agricultural landscapes. Nova Science Publishers, New York, p. 143-160.). Moreover, environmental education programs directed at wildlife could orientate populations as well as assist in the conservation of the species in rural landscapes.

CONCLUSION

The present findings show that the residents of rural communities interviewed demonstrate knowledge regarding C. thous as well as its ecological, morphological and utilitarian characteristics. The findings also suggest that its adaptability and use of different resources enable C. thous to take advantage of rural landscapes.

According to the respondents, due to its negative roles as a wild animal, predator of small domesticated animals and a threat to health, the crab-eating fox is the main carnivore that causes conflicts with rural communities by attacking domesticated animals that are a source of income and food for local families. However, the positive roles for C. thous cited were use for medicinal purposes, craftwork, mystical-religious activities and as a pet. Thus, it is important to understand the relationship between the population studied and C. thous used as a faunal resource, as this is a wild animal that is submitted to other pressures, taking into consideration biological, conservationist and cultural aspects.

The findings demonstrate a need for further information on this animal as well as adequate measures to reduce contact between the species and local communities in an effort to ensure the preservation of the species and diminish conflicts related to the predation of domesticated animals and the transmission of rabies. Environmental education actions should be implemented to inform local communities with regard to the importance of C. thous to the balance of the ecosystem and public health issues, serving as a useful tool for conservation programs and the achievement of sustainable societies.

ACKNOWLEGMENTS

The authors are grateful to all respondents who shared their knowledge in this study.

REFERENCES

  • ABREU JÚNIOR EF & KOHLER A. 2009. Mastofauna de médio e grande porte na RPPN da UNISC. Biota Neotrop 9: 169-174.
  • ALBUQUERQUE UP & ANDRADE LHC. 2002. Uso de recursos vegetais da caatinga: o caso do agreste do estado de Pernambuco (Nordeste do Brasil). Interciencia 27: 336-346.
  • ALEXANDER B, CARVALHO RL, CALLUM MCH & PEREIRA MH. 2002. Roler of the domestic chicken (Gallus gallus) in the epidemiology of urban visceral leishmaiasis in Brasil. Emerg Infect Dis 8: 1480-1485.
  • ALVES MM, LOPES SF & ALVES RRN. 2016. Wild Vertebrates kept as pets in the semiarid region of Brasil. Trop Conserv Sci 9: 354-368.
  • ALVES RRN, LIMA JRF & ARAÚJO HF. 2013. The live bird trade in Brazil and its conservation implications: an overview. Bird Conserv Int 23: 53-65.
  • ALVES RRN, MENDONÇA LET, CONFESSOR MVA, VIEIRA WLS & LOPES LCS. 2009. Hunting strategies used in the semi-arid region of northeastern Brazil. J Ethnobiol Ethnomed 5: 1-16.
  • ALVES RRN & SOUTO WMS. 2010. Etnozoologia: conceitos, considerações e importância. In: Alves RRN et al. (Eds), Etnozoologia no Brasil: importância, status atual e perspectivas. NUPEEA. Recife, p. 21-40.
  • ANTUNES KD ET AL. 2018. Descriptive analysis of rabies in wild animals in the state of Sergipe, Brazil. Arq Bras Med Vet Zootec 70: 169-173.
  • ATHREYA V, ODDEN M, LINNELL JDC, KRISHNASWAMY J & KARANTH U. 2013. Big Cats in Our Backyards: Persistence of Large Carnivores in a Human Dominated Landscape in India. PLoS ONE 8: e57872.
  • BARBOSA A, OLIVEIRA DSC & OLIVEIRA CRM. 2014. Uso tradicional da fauna silvestre do município de Lapão Bahia. Enciclopédia Biosfera 10: 118-133.
  • BARBOSA JAA & AGUIAR JO. 2012. Utilização místico-tradicional da fauna no semiárido paraibano, Paraíba, Brasil. Polêm!ca 11: 642-649.
  • BARBOSA JAA & AGUIAR JO. 2015. Conhecimento e usos da fauna por caçadores no semiárido brasileiro: Um estudo de caso no estado da Paraíba, Nordeste do Brasil. Biotemas 28: 137-148.
  • BEISEIGEL BM, LEMOS FG, AZEVEDO FC, QUEIROLO D & JORGE RS. 2013. Avaliação do risco de extinção do cachorro-do-mato Cerdocyon thous (Linnaeus, 1766) no Brasil. Instituto Chico Mendes de Conservação da Biodiversidade, p. 138-143.
  • BELTRÁN J & DELIBES M. 1994. Environmental determinants of circadian activity o free-ranging Iberian lynxes. J Mammal 75: 382-393.
  • BERNARD HR. 1994. Research Methods in: Anthropology: Qualitative and Quantitative Approaches. Sage. Thousand Oaks, CA, EEUU, p. 824.
  • BERNARDI F, NADIN-DAVIS SA, WANDELER AI, ARMSTRONG J, GOMES AAB, LIMA FS, NOGUEIRA FR & ITO FH. 2005. Antigenic and genetic characteization of rabies viroses isolated from domestic and wild animals of Brazil identifies the hoary fox as a rabies reservoir, J Gen Virol 86: 3153-3162.
  • CERQUEIRA EJL, SILVA EM, MONTE-ALEGRE AF & SHERLOCK IA. 1998. Considerações sobre pulgas (Siphonaptera) da raposa Cerdocyon thous (Canidae) da área endêmica de leishmaniose visceral de Jacobina, Bahia, Brasil. Rev Soc Bras Med Tro 33: 91-93.
  • CHIARELLO AG. 1999. Effects of fragmentation of the Atlantic forest on mammal communities in southeastern Brazil. Biol Conserv 89: 71-82.
  • CHIEREGATTO A, CALZOLARI F, TRASFORINI G, TARGA L & LATRONICO N. 2003. Normal jugular bulb oxygen saturation. J Neurol Neurosur Ps 74: 784-786.
  • COURTENAY O & MAFFEI L. 2004. Crab-eating Fox Cerdocyon thous. In: Sillero-Zubiri C et al. Canids: foxes, wolves, jackals and dogs. Status survey and conservation action plan, IUCN / SSC Canid Specialist Group, IUCN, Gland, Switzerland and Cambridge, UK, p. 32-38.
  • CPRM. 2005. Serviço geológico do Brasil. Mapa geológico do Estado de Pernambuco. Ministério de Minas e Energia- Secretária de Mineração e transformação mineral. Brasília. Disponível em: < http://www.cprm.gov.br>. Acesso em 22 de junho de 2018.
    » http://www.cprm.gov.br
  • CRUZ MAOM, BORGES-NOJOSA DM, LANGGUTH AR, SOUZA MAN, SILVA LAM, LEITE LMRM, PRADO FMV, VERÍSSIMO KCS & MORAES BLC. 2002. Diversidade de mamíferos em áreas prioritárias para conservação da caatinga, p. 182-226.
  • DIAS DM, RIBEIRO AS, BOCCHIGLIERI A & PEREIRA TC. 2014. Diversidade de carnívoros (mammalia: carnivora) da serra dos macacos, Tobias Barreto, Sergipe. Biosci J 30: 1192-1204.
  • FAHRIG L. 2003. Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Evol Syst 34: 487-515.
  • FERREIRA AS, PERES CA, BOGONI JÁ & CASSANO CR. 2018. Use of agroecosystem matrix habitats by mammalian carnivores (Carnivora): a global-scale analysis. Mamm Rev 48: 312-327.
  • GARCÍA-GRAJALES J. 2013. El conflicto hombre-cocodrilo en México: causas e implicaciones. Interciencia 38: 881-884.
  • GIBSON JJ. 1979. The Ecological Approach to Visual Perception. Boston: Houghton Mifflin, Boston, 332 p.
  • IBGE - INSTITUTO BRASILEIRO DE GEOGRAFIA E ESTATÍSTICA. 2018. Censo Populacional 2010. Disponível em: <https://cidades.ibge.gov.br/brasil/pe/panorama> último acesso 18 de julho de 2018.
    » https://cidades.ibge.gov.br/brasil/pe/panorama
  • INMET - INSTITUTO NACIONAL DE METEOROLOGIA. 2015. Disponível em: <www.inmet.gov.br/portal/index.php?r=home2/pageepage>. Disponível em 06 de abril de 2015.
    » www.inmet.gov.br/portal/index.php?r=home2/pageepage
  • JORGE RSP, ROCHA FL, MAY JA & MORATO RG. 2010. Ocorrência de patógenos em carnívoros selvagens brasileiros e suas implicações para a conservação e saúde pública. Oecol Aust 14: 686-710.
  • JUAREZ KM & MARINHO-FILHO J. 2002. Diet, habitat use, and home ranges of sympatric canids in Central Brazil. J Mammal 83: 925-933.
  • KASPER CB, FELDENS MJ, MAZIM FD, SCHNEIDER A, CADEMARTORI CV & GRILLO HCZ. 2007. Mamíferos do Vale do Taquari, Região Central do Rio Grande do Sul. Biocienc 15: 53-62.
  • KOTAIT I, CARRIERI ML, CARNIELI JRP, CASTILHO JG, OLIVEIRA RN, MACEDO CI, FERREIRA KCS & ACHKAR SM. 2007. Reservatórios silvestres do vírus da raiva: um desafio para a saúde pública. BEPA, Bol Epidemiol Paul 4: 02-08.
  • LEMOS FG, AZEVEDO FC, COSTA HCM & JUNIOR JAM. 2011b. Human threats to hoary and crab-eating foxes in central Brazil. Canid News 14: 1-6.
  • LEMOS FG, FACURE KG & AZEVEDO FCA. 2011a. First approach to the comparative ecology of the hoary fox and the crab-eating fox in a fragmeted human altered landscape in the Cerrado biome at central Brasil. In: Rosalino LM & Costa-Gheler C. Middle-sized carnivores in agricultural landscapes. Nova Science Publishers, New York, p. 143-160.
  • LICARIÃO MR, BEZERRA DMM & ALVES RRN. 2013. Wild birds as pets in Campina Grande, Paraíba State, Brazil: An Ethnozoological Approach. An Acad Bras Cienc 85: 201-213.
  • MAFFEI L & TABER AB. 2003. Área de acción, actividad y uso de hábitat del zorro patas negras, Cerdocyon thous, en un bosque seco. Mastozool Neotrop 10: 154-160.
  • MARQUES JGW. 2001. Pescando pescadores: Ciência e Etnociência em uma Perspectiva Ecológica. NUPAUB, USP. São Paulo, Brasil, p. 258.
  • MATSON PA, PARTON WJ, POWER AG & SWIFT MJ. 1997. Agricultural intensification and ecosystem properties. Science 277: 504-509.
  • MENDONÇA LET, SOUTO CM, ANDRELINO LL, SOUTO WMS, VIEIRA WLS & ALVES RRN. 2011. Conflitos entre pessoas e animais silvestres no Semiárido paraibano e suas implicações para conservação. Sitientibus Ser Cienc Biol 11: 185-199.
  • MICHALSKI F, BOULHOSA RLP, FARIA A & PERES CA. 2006. Human–wildlife conflicts in a fragmented Amazonian forest landscape: determinants of large felid depredation on livestock. Anim Conserv 9: 179-188.
  • MUELLER CC. 1996. Organização e ordenamento do espaço regional do Nordeste. Planejamento e Políticas Públicas, IPEA n.13, p. 35-111.
  • NOWELL K & JACKSON P. 1996. Wild Cats. Status Survey and Conservation Action Plan. IUCN/SSC Cat Specialist Group, Gland, Switzerland.
  • ONDERDONK D & CHAPMAN C. 2000. Coping with forest fragmentation: The primates of Kibale National Park, Uganda. Int J Primatol 21: 587-611.
  • PEZZUTI J & CHAVES RP. 2009. Etnografia e manejo de recursos naturais pelos índios Deni, Amazonas, Brasil. Acta Amaz 39: 121-138.
  • REIS NR, PERACCHI AL, PEDRO WA & LIMA IP. 2006. Mamíferos do Brasil. Londrina, p. 437.
  • ROCHA VJ, REIS NR & SEKIAMA ML. 2004. Dieta e dispersão de sementes por Cerdocyon thous (Linnaeus) (Carnívora, Canidae), em um fragmento florestal no Paraná, Brasil. Rev Bras Zool 21: 871-876.
  • SANTOS MFM, PELLANDA M, TOMAZZONI AC, HASENACK H & HARTZ SM. 2004. Mamíferos carnívoros e sua relação com a diversidade de hábitats no Parque Nacional dos Aparados da Serra, sul do Brasil. Iheringia Sér Zool 94: 235-245.
  • STAHL PW. 2012. Interactions between humans and endemic canids in Holocene South America. J Ethnobiol 32: 108-127.
  • TABARELLI M, MELO MDVC & LIRA OC. 2006. A Mata Atlântica do nordeste. In: Campanili M & Prochnow M (Eds). Mata Atlântica - uma rede pela floresta. RMA, Brasília, p. 1-17.
  • TILMAN D, FARGIONE J, WOLFF B, D’ANTONIO C, DOBSON A, HOWARTH R, SCHINDLER D, SCHLESINGER WH, SIMBERLOFF D & SWACKHAMER D. 2001. Forecasting agriculturally driven global environmental change. Science 292: 281-284.
  • VANAK AT & GOMPPER ME. 2010. Interference competition at the landscape level: the effect of free-ranging dogs on a native mesocarnivore. J Appl Ecol 47: 1225-1232.
  • WADA MY, ROCHA SM & MAIA-ELKHOURY ANS. 2011. Situação da raiva no Brasil, 2000 a 2009. Epidemiol Serv Saúde 20: 509-518.
  • WOODROFFE R & GINSBERG JR. 1998. Edge effects and the extinction of populations inside protected areas. Science 280: 2126-2128.

Publication Dates

  • Publication in this collection
    02 Dec 2020
  • Date of issue
    2020

History

  • Received
    28 Aug 2018
  • Accepted
    15 Apr 2019
Academia Brasileira de Ciências Rua Anfilófio de Carvalho, 29, 3º andar, 20030-060 Rio de Janeiro RJ Brasil, Tel: +55 21 3907-8100 - Rio de Janeiro - RJ - Brazil
E-mail: aabc@abc.org.br