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Iheringia. Série Zoologia

Print version ISSN 0073-4721On-line version ISSN 1678-4766

Iheringia, Sér. Zool. vol.109  Porto Alegre  2019  Epub Nov 11, 2019

https://doi.org/10.1590/1678-4766e2019036 

Article

Roadkilled mammals in the northern Amazon region and comparisons with roadways in other regions of Brazil

Mamíferos atropelados na região norte da Amazônia e comparações com rodovias de outras regiões do Brasil.

Heloisa S. Caires1 
http://orcid.org/0000-0002-0664-7468

Cleide R. Souza2 
http://orcid.org/0000-0003-2001-6790

Débora N. C. Lobato3 
http://orcid.org/0000-0003-2696-023X

Marília N. S. Fernandes4 
http://orcid.org/0000-0002-6333-6471

Júnio S. Damasceno3  5 
http://orcid.org/0000-0001-9282-221X

1Centro Universitário Luterano de Ji-Paraná (CEULJI/ULBRA), Av. Eng. Manfredo Barata Almeida da Fonseca, 762, 76907-438 Ji-Paraná, RO, Brazil.

2Instituto Chico Mendes (ICMBIO), Av. Lauro Sodré, 6500, 76803-260 Porto Velho, RO, Brazil.

3Universidade do Estado de Minas Gerais (UEMG), Unidade Divinópolis, Rua Paraná, 3001, 35501-170 Divinópolis, MG, Brazil. (jdamascenobh@gmail.com)

4Universidade Federal de Minas Gerais (UFMG), Av. Pres. Antônio Carlos, 6627, 31270-901 Belo Horizonte, MG, Brazil.

5Universidade do Estado de Minas Gerais (UEMG), Unidade João Monlevade, Av. Laranjeiras, 314, 35930-330 João Monlevade, MG, Brazil.


ABSTRACT

Roadways and road traffic modify landscapes, posing a threat to the conservation of species in different biomes. The aim of the present study was to analyze roadkill records of wild mammals and to compare the results to findings from 37 other studies conducted in Brazil, to evaluate the richness and diversity of threatened species in different eco-regions of the country. This study was conducted between June 2007 and June 2008, along 60 km of the inter-state highway BR-364, which connects the municipalities of Ouro Preto d’Oeste and Presidente Médici in the state of Rondônia (northern Brazil). Two hundred twenty roadkills were recorded involving 13 species of mammals. Cingualata, Pilosa and Carnivora were the most represented orders. The most represented were the generalist species Dasypus novemcinctus (56.7%), Tamandua tetradactyla (10.5%), and Cerdocyon thous (8.2%), reflecting the adaptability of these species to habitat changes and presence of humans. The number of roadkilled individuals and species indicated no significant differences between the dry and rainy seasons. The findings indicate a high index of roadkills (3.38 individuals/km/year) and moderate number of run over species (0.20 species/km/year) in the region in comparison to records from other roadways in Brazil, with 46% species having an endangered status. Roadways in the eco-regions of the Cerrado (Brazilian savanna) accounted a significantly larger proportion of endangered species (mean: 52%) in comparison to the Pampa (lowlands of southern Brazil; 24%), but the differences in comparison to roadways in Amazonia (37%) and the Atlantic Forest (31%) were non-significant. The present findings underscore the need for emergency measures to minimize the impact of roadkills on mammals. Moreover, priority should be given to more impacted roadways and more threaten eco-regions.

KEYWORDS Environmental impact; habitat fragmentation; hotspots; threatened wildlife

RESUMO

As rodovias e o fluxo de veículos contribuem para os processos de fragmentação da paisagem e alteração do habitat natural, representando ameaça para conservação das espécies em diversos biomas. Este estudo avalia os registros de atropelamentos das espécies de mamíferos silvestres e compara este com outros 37 estudos realizados no Brasil, para avaliar a riqueza e diversidade de espécies ameaçadas em distintas ecorregiões. O estudo foi realizado entre junho de 2007 e junho de 2008, ao longo de 60 km da rota BR-364, entre os municípios de Ouro Preto d’Oeste e Presidente Médici, no estado de Rondônia. Foram registrados 220 atropelamentos pertencentes a 13 espécies de mamíferos. Cingualata, Pilosa e Carnivora foram as ordens mais representadas, sendo Dasypus novemcinctus a espécie mais significativa (56.7%), seguida por Tamandua tetradactyla (10.5%) e Cerdocyon thous (8.2%), refletindo a capacidade de adaptação das espécies às alterações do habitats e a presença humana. O número de atropelamentos de indivíduos e espécies não indicaram diferenças significativas entre estações climáticas. Este estudo indica altos índices de atropelamentos de indivíduos (3.38 indivíduos/km/ano) e moderado número de espécies atropeladas (0.20 espécies/km/ano) para a região em relação a outras localidades no Brasil, com 46% das espécies em status de ameaça. As rodovias nas ecorregiões do Cerrado apresentaram resultados significativamente maiores de espécies ameaçadas (média de 52%) em relação ao Pampa (24%), porém não houve diferença significativa se comparado às rodovias na Amazônia (37%) e Mata Atlântica (31%). Os dados reforçam a necessidade de medidas emergenciais para minimizar impactos por atropelamentos da mastofauna, recomendando prioridade em rodovias mais impactadas e ecorregiões mais ameaçadas.

PALAVRAS-CHAVE Impacto ambiental; fragmentação de habitat; hotspots; fauna ameaçada

Roadways through Amazon habitats are determinant factors of vast deforestation patterns and forest fragmentation related to the expansion of agriculture, lumber and pasture activities, and these aspects are more intensified by clandestine secondary roads (Fearnside, 2015). Roadways also alter the physical, chemical and biological patterns of terrestrial and aquatic environments, affecting drainage, infiltration and evaporation patterns, with direct consequences to the microclimate in areas surrounding these transportation lanes (Laurance et al., 2009).

Although there is no consensus on the effect of seasonality on mammals killed by vehicular traffic (Carvalho et al., 2017), studies demonstrate a correlation between vehicle-related deaths (roadkills) of wild mammals and seasonality (Brum et al., 2017), which is likely associated with dispersal and migration movements related to foraging and reproduction (Braz & França, 2016).

Roads serve as barriers to animal movements between forest fragments (Tumeleiro et al., 2006) and constitute a potential risk for the occurrence of roadkills, especially on roadways with high traffic flow passing through areas that serve as refuge for wild animals (Vieira, 1996).

Deforestation and habitat destruction in the Amazon basin have been associated with the proximity to roadways, especially towards the southeast of this biome, with the Belém-Brasília highway (BR-010), Trans-Amazonia highway (BR-319), and BR-364 playing important roles (Laurence et al., 2002). Roadway BR-364 in the state of Rondônia has a high vehicular traffic flow and crosses one of the regions with the highest rates of deforestation for conversion into pastures as well as the strongest pressures stemming from human occupation in the Amazon (Fearnside, 2006). The isolation of populations and habitat fragmentation caused by deforestation intensify the occurrence of mammals on roadways and promote changes in the behavior of species. Such changes increase the mortality rate due to roadkills and the limitations imposed on the availability of resources, even for discreet, reclusive species that avoid roads and open areas (Trombulak & Frissel, 2000).

The aims of the present study were to identify large and medium-sized mammals that have been victims of roadkill along a stretch of federal roadway BR-364 in the state of Rondônia (northern Brazil), to evaluate the potential of environmental effects (temperature and precipitation) on the occurrence of roadkill in the stretch analyzed, to perform a comparative analysis of the study area and roadkill records of wild mammals in other regions of Brazil based on the available literature, and to identify priority regions and biomes for conservation.

MATERIAL AND METHODS

Study area. The study area comprised the 60-km stretch of the BR-364 between the municipalities of Ouro Preto do Oeste (10°S, 62°W) and Presidente Médici (11°S, 61°W) in the state of Rondônia, which are equidistant from the municipality of Ji-Paraná (Fig. 1).

Fig. 1 Study area located on roadway BR 364 in central region of state of Rondônia in southwestern portion of Amazon biome. The stretch sampled is in bold in the figure. 

The stretch of the roadway studied is paved and passes through a matrix of pastures and isolated fragments of natural and secondary rainforest under strong human pressure, between large indigenous reserves and some conservation units, with remaining areas having a low degree of species regeneration of the primitive vegetation (Lisboa et al., 1991). The study area is located at the southern limit of the Amazon rainforest (Amazonia) near its transition area to the Cerrado (savanna) eco-region located in the southern portion of the state of Rondônia (Miranda et al., 2006).

Sampling. Sampling was performed between June 2007 and June 2008, covering a 60-km stretch of the central region of roadway BR-364, between the municipalities of Presidente Médici (south) to Ouro Preto D’Oeste (north). To locate dead mammals along the roadway, 22 trips totaling 1320 km were performed by two observers on a motorcycle traveling at 15-day intervals, preferably in the morning period, at an approximate velocity of 50 km/h (Sousa & Miranda, 2010; Corrêa et al., 2017). Roadkilled mammals within urban areas of municipalities, deaths by unknown causes and the carcasses of domesticated animals were not quantified in this study (Hengemühle & Cademartori, 2008).

The specimens were photographed and identified by external characteristics with the aid of a taxonomic key (Emmons & Feer, 1997) and identification guides (Borges & Tomás, 2004; Reis et al., 2006). Small rodents (N = 4) and bats (N = 23) were not included in the analyses, but marsupials, such as Didelphis Linnaeus, 1758, were included due to the ease to identify them in the field. Non-identified specimens (N = 2) and exotic species (N = 6) were not considered in the calculation of species and roadkill rates on roadways.

For the evaluation of roadways with the highest roadkill rates in Brazil, bibliographic searches were performed in Google, Google Scholar, the SciELO site, and the Brazilian periodical site Portal da Capes, for studies addressing roadkilled wild fauna on Brazilian roadways, using the following search terms: “atropelamento de mamíferos”, “roadkill mammals”, “vertebrates roadkill” and “wildlife roadkill”. We only considered studies on roads in Brazil that discriminated the distance in kilometers travelled, duration of the study in months, and number of individuals and species of large and medium-sized mammals, excluding domesticated and exotic animals. For each article selected (N = 37), stretches of roadways were included in the main eco-regions of the country: Amazon rainforest (Amazonia), tropical dry forest (Caatinga), savanna (Cerrado), coastal rainforest (Atlantic Forest), lowlands in the southern region of the country (Pampa), and wetlands in the central-western region of the country (Pantanal) (MMA, 2002).

Data analysis. Relative abundance was estimated based on the percentage of absolute records of roadkilled individuals of each species: relative abundance of a given species = absolute n° of individuals of a given species x 100 / total n° of roadkilled animals. Relative abundances of each species were compared between the dry season (May to October) and rainy season (November to April). The Mann-Whitney test was used to determine seasonal differences with a 5% level of significance.

For each season (dry and rainy), precipitation and temperature data from the closest meteorological station were acquired from the National Meteorological Institute (www.inmet.gov.br). Pearson’s test was used to evaluate the correlation between the climatic data and the ecological variables (number of individuals and number of species) using the BioEstat 5.3 software (Ayres et al., 2007).

The degree of impact of the stretch analyzed in comparison to other roadways analyzed in previous studies was determined based on the roadkill rate calculated by the number of individuals and species divided by total kilometers travelled (adapted from Carvalho et al., 2014). The mean was obtained from the total of individuals and species divided by total kilometers travelled. For the comparison of data, the results were subsequently divided by the total number of sampling months multiplied by 12 to standardize the individual (individual roadkill index [IRI]) and species (species roadkill index [SRI]) roadkilled in a one-year period for each study. The mean general IRI and SRI were calculated by the sum of all values of each index divided by the number of studies analyzed.

The species identified in the 37 papers included in the bibliographic review and those from the present study were categorized based on the degree of endangerment [extinct in the wild (EW), critically endangered (CR), endangered (EN), and vulnerable (VU)], using official lists of endangered species (Bergallo et al., 2000; Marques et al., 2002; Fontana et al., 2003; Mickich & Bernils, 2004; Passamani & Mendes, 2007; Drummond et al., 2008; Percequillo & Kierulff, 2009; COPAM, 2010; MMA, 2014; IUCN, 2018).

The ratio EN/ST in each study was determined based on the number of endangered species (EN) divided by the total number of mammals (ST) listed in each study.

The comparative analysis of the roadkill records in the different eco-regions was performed applying the Kruskal-Wallis test, followed by Dunn’s test for significant results (p < 0.05) in the BioEstat 5.3 software (Ayres et al., 2007). The Caatinga and Pantanal biomes had few studies and were therefore excluded from the comparisons with the other eco-regions (Amazonia, Cerrado, Atlantic Forest and Pampa).

RESULTS

Two hundred twenty roadkilled wild mammals were recorded over the 1320 km traveled, corresponding to 3.38 individuals/km/year (IRI) during the study period. These mammals represented a total of 13 species (Fig. 1).

The orders Cingulata and Pilosa were the most represented, accounting for nearly 68% of the roadkill occurrences (Tab. I). The order Carnivora accounted for 19% of the roadkill records and the order Didelphimorphia was the third most represented in the study (Tab. I). In terms of species, the nine-banded armadillo (Dasypus novemcinctus) accounted for 57% of the roadkilled mammals, followed by the lesser anteater (Tamandua tetradactyla, 10.5%), crab-eating fox (Cerdocyon thous, 8.2%), crab-eating raccoon (Procyon cancrivorus, 5.9%) and common opossum (Didelphis marsupialis, 6.4%) (Tab. I).

Tab. I Roadkilled mammals on roadway BR-364 between municipalities of Presidente Médici (PM) and Ouro Preto do Oeste (OP) in state of Rondônia between June 2007 and June 2008 (Nra, roadkill records of each species in rainy season; Ndr, roadkill records of each species in dry season; %, roadkill frequency based on total number of individuals). 

Taxonomic group Popular name Nra Ndr %
MAMMALIA
Didelphimorphia
Didelphidae
Didelphis marsupialis Linnaeus, 1758 Opossum 5 9 6.4
Cingulata
Dasypodidae
Dasypus novemcinctus Linnaeus, 1758 Nine-banded armadillo 89 36 56.8
Pilosa
Bradypodidae
Bradypus variegatus Schinz, 1825 Three-toed sloths 1 1 0.9
Myrmecophagidae
Tamandua tetradactyla Linnaeus, 1758 Lesser anteater 12 11 10.4
Primata
Cebidae
Saimiri sciureus (Linnaeus, 1758) Common squirel monkey 0 2 0.9
Carnivora
Felidae
Leopardus braccatus (Cope, 1889) Pantanal cat 0 2 0.9
Canidae
Cerdocyon thous (Linnaeus, 1766) Crab-eating fox 5 13 8.2
Procyonidae
Nasua nasua (Linnaeus, 1766) Coatis 3 0 1.4
Procyon cancrivorous (Cuvier, 1798) Crab-eating raccoon 7 6 5.9
Mustelidae
Eira barbara Linnaeus, 1758 Tayra 3 2 2.3
Rodentia
Hydrochaeridae
Hydrochaerus hydrochaeris (Linnaeus, 1766) Capybara 4 0 1.8
Cuniculidae
Cuniculus paca (Linnaeus, 1766) Spotted paca 3 0 1.4
Erethizontidae
Coendou prehensilis (Linnaeus, 1758) Porcupine 2 4 2.7
134 86 100
TOTAL 220

Although the rainfall data indicated significant differences in the precipitation volume between the dry (May to October) and rainy (November to April) seasons (U = 2.00; Z[U] = 2.56; p = 0.0104), the temperature and rainfall data were not correlated with the number of individuals (temperature: r = 0.0564, p = 0.8617; rainfall: r = 0.0677, p = 0.8343) or number of species (temperature: r = 0.0574, p = 0.8594; rainfall: r = -0.3088, p = 0.3288).

Comparison of Brazilian roadways. The bibliographic review and the present study resulted in 38 papers distributed among the six eco-regions of Brazil; Amazonia (N = 6), Caatinga (N = 2), Cerrado (N = 9), Atlantic Forest (N = 14), Pampa (N = 6) and Pantanal (N = 1) (Fig. 2). The roadkill indices on Brazilian roads ranged from 0.12 to 5.5 individuals per kilometer per year (IRI), with a mean of 1.47 (IRI), and from 0.01 to 1.67 species per kilometer per year (SRI), with a mean of 0.27 (SRI).

Fig. 2 Number of articles evaluated with records of the 13 species identified in this study and the distribution in each of the six Brazilian eco-regions (Amazonia, Caatinga, Cerrado, Atlantic rainforest, Pampa and Pantanal). 

Among the 13 species recorded in the present study, the crab-eating fox (33 papers: 87%) was the most frequently reported species in the 38 articles, followed by the nine-banded armadillo (27 papers: 71%), crab-eating raccoon (22 papers: 58%) and lesser anteater (20 papers: 53%). The common squirrel monkey was only recorded in the present study (Fig. 2).

Roadkill index: number of records, number of species and ratio of endangered species. The data from different roadways in Brazil indicate that roadway BR-364 has a comparatively high roadkill index based on the number of individuals and number of endangered mammals killed. The stretch of BR-364 had the sixth highest index for large and medium-sized mammals (IRI = 3.38) among the 38 studies involving different roadways in the country. This index was more than twice the national average (IRI = 1.47) (Tab. II).

Tab. II Comparison of roadkill indices among Brazilian roadways based on number of records per year (IRI), species per year (SRI), eco-regions of sampled stretch of road, and ratio between endangered species and total species (ES/TS), in 38 references considering large and medium-sized mammals. 

References Unit of federation Eco-region IRI SRI EN/TS
This study RO Amazon Rainforest 3.38 0.20 0.46
Almeida & Cardoso-Junior, 2014 SP Atlantic Forest 1.74 0.41 0.00
Braz & França, 2016 GO Brazilian Savanna 0.94 0.10 0.62
Brum et al., 2017 MT Brazilian Savanna 2.52 0.36 0.61
Caceres et al., 2010 MS Atlantic Forest 3.50 0.30 0.53
Caceres et al., 2010 MS Brazilian Savanna 1.06 0.07 0.65
Caceres et al., 2012 MS Wetland 0.47 0.06 0.40
Caceres et al., 2012 MS Brazilian Savanna 0.53 0.06 0.61
Carvalho et al., 2014 MS Brazilian Savanna 0.37 0.07 0.50
Cherem et al., 2007 SC Atlantic Forest 0.12 0.01 0.40
Corrêa et al., 2017 RS Brazilian Pampa 3.11 0.44 0.40
Costa & Dias, 2013 GO Brazilian Savanna 1.33 0.24 0.36
Costa, 2011 SC Atlantic Forest 0.90 0.24 0.20
Cunha et al., 2010 GO Brazilian Savanna 0.86 0.06 0.35
Cunha et al., 2015 RS Brazilian Pampa 5.50 1.67 0.20
Deffaci et al., 2016 RS Atlantic Forest 4.25 0.58 0.14
Gumier-Costa & Sperber, 2009 PA Amazon Rainforest 0.91 0.14 0.50
Hegel et al., 2012 RS Atlantic Forest 1.57 0.30 0.38
Hengemühle & Cademartori, 2008 RS Brazilian Pampa 3.50 0.90 0.22
Machado et al., 2015 MG Atlantic Forest 0.89 0.27 0.17
Melo & Santos-Filho, 2007 MT Brazilian Savanna 1.89 0.24 0.47
Milli & Passamani, 2006 ES Atlantic Forest 0.64 0.21 0.50
Oliveira et al., 2017 MG Brazilian Savanna 0.88 0.23 0.50
OmenaJr. et al., 2012 AM Amazon Rainforest 0.76 0.05 0.40
Orlandin et al., 2015 SC Atlantic Forest 0.40 0.07 0.38
Pereira et al., 2006 PA Amazon Rainforest 0.61 0.08 0.33
Pinheiro & Turci, 2013 AC Amazon Rainforest 1.77 0.55 0.25
Preuss et al., 2015 SC Atlantic Forest 1.09 0.10 0.43
Ramos-Abrantes et al., 2018 PB Tropical Dry Forest 0.58 0.04 0.29
Rosa & Mauhs, 2004 RS Brazilian Pampa 0.41 0.09 0.00
Santana, 2012 RS Brazilian Pampa 0.86 0.04 0.31
Santos et al., 2012 MG Atlantic Forest 0.92 0.46 0.33
Saranholi et al., 2016 SP Atlantic Forest 0.75 0.52 0.55
Sássi et al., 2013 MG Atlantic Forest 1.06 0.09 0.30
Silva et al., 2013 RS Brazilian Pampa 4.03 0.41 0.33
Sousa & Miranda, 2010 PB Atlantic Forest 0.36 0.04 0.00
Turci & Bernarde, 2009 RO Amazon Rainforest 0.54 0.05 0.20
Veras et al., 2016 PI Tropical Dry Forest 1.00 0.50 0.00
BRAZIL MEAN 1.47 0.27 0.34

The stretch of the BR-364 ranked sixteenth with regard to the roadkilled species index (SRI = 0.20) among the 38 roadways evaluated. This index was close to the national average (SRI = 0.27). The stretch of BR-364 ranked 12th with regard to the number of endangered species, with 46% of the species listed in some endangered category.

Comparison of eco-regions. No significant differences among eco-regions were found regarding the number of records or number of species (km/year). Regarding the ratio of endangered species recorded in each eco-region, the Cerrado (savanna) had significantly higher occurrences in comparison to the Pampa (H = 9.5011; G.L. 3; p = 0.0233), with an average of 52% and 24% of the roadkill records, respectively. The Pantanal (wetlands) and Caatinga (tropical dry forest), which were not included in the statistical analysis, had proportions of 40% and 15%, respectively.

DISCUSSION

The higher roadkill rates of large and medium-sized mammals for the stretch of BR-364 studied (IRI = 3.38) in the state of Rondônia may be explained by the high vehicle traffic for the flow of cargo associated with the fragmentation and loss of natural habitats. Moreover, the state of Rondônia is situated in Amazonia, with a recent history of intensive deforestation and fragmentation of areas, associated mainly with the paving of roadway BR 364 (Fearnside, 2005; Sathler et al., 2018). Therefore, animals are more exposed to the risk of being killed by vehicular traffic due to their use of roadways as simpler routes to follow in search of new habitats given the limitation of natural areas and the opportunity to exploit new food resources made available by the roads.

The high roadkill indices for D. novemcinctus, T. tetradactyla, C. thous, D. marsupialis and P. cancrivorous in this study demonstrate that the occurrence of these species is relatively common in different eco-regions. Species of Cingulata, Pilosa and Carnivora are largely generalists and have broad distribution, with records in several regions of Brazil (Pereira et al., 2006; Melo & Santos-Filho, 2007; Caceres et al., 2010; Machado et al., 2015; Ramos-Abrantes et al., 2018). These animals are also exposed to frequent roadway crossings due to their necrophagous habits (Scoss et al., 2004). Moreover, some species may experience a population increase in highly fragmented habitats. As generalist species tend to be invasive and opportunistic, they have greater success in terms of establishment and expansion in areas with inferior environmental quality (Marvier et al., 2004).

The high roadkill rate of the nine-banded armadillo may be related to its opportunistic capacity to adapt to the conditions of the environment (Redford, 1994). This animal is a generalist insectivore that is abundant in forest fragments and the edges of forests (Loughry & McDounough, 1997). Roadkill records may also be associated with aggregations in reproductive periods (Clevenger et al., 2003).

The lesser anteater is adapted to a large variety of habitats (Redford, 1994). However, this animal is very selective in its choice of habitat and is dependent on forest cover and wet areas (Desbiez et al., 2009). The high frequency of roadkill records (Cherem et al., 2007; Cunha et al., 2010; Costa, 2011; Caceres et al., 2012) may be due to its limited sight and hearing as well as its exposure during slow movements between forest fragments intercepted by roadways (Brum et al., 2017).

The crab-eating fox is a nocturnal carnivore in Neotropical regions with a large home range and high capacity for an opportunistic, generalist, omnivorous diet (Cheida et al., 2006). High occurrences of roadkill affecting the crab-eating are found in diverse regions (Pereira et al., 2006; Cherem et al., 2007; Caceres et al., 2010; Caceres et al., 2012; Costa & Dias, 2013; Carvalho et al., 2014; Brum et al., 2017; Ramos-Abrantes et al., 2018), which reflects its highly mobile behavior, exposing the animal during its constant crossings of roadways associated to its necrophagous diet (Melo & Santos-Filho, 2007; Sousa & Miranda, 2010).

The crab-eating raccoon is a solitary species with nocturnal habits and broad distribution (Cheida et al., 2006). This animal occupies a large variety of habitats, travels large distances and is tolerant to human disturbances (Arispe et al., 2008). It depends on areas with sources of water and is vulnerable to the destruction of forest corridors, preferring to travel along open paths and trails in the vegetation (Trolle & Kéry, 2005). Indeed, the occurrence of this species in roadkill fauna is very common in Brazil (Cherem et al., 2007; Caceres et al., 2012; Preuss, 2015).

The common opossum occurs in both natural and human-altered habitats, with the ability to adapt well to large urban centers (Cordero-Rodriguez, 2000). High roadkill rates are found in different regions of Brazil (Gumier-Costa & Sperber, 2009; Omena-Junior et al., 2012; Sássi et al., 2013), which may be related to the attraction of this animal to carcasses on roadways. The common opossum adapts to different types of climate, vegetation and diet, exploiting a wide range of environments, including demarcated human routes (Vaughan & Hawkins, 1999).

The process of changes in the original forest cover occurring in the region has favored species with opportunistic habits and has maintained species more dependent on the forest environment. Moreover, generalist omnivorous mammals benefit from their adaptability and plasticity, but are also more vulnerable to being struck by vehicles due to their attraction to a broad gamut of food sources, which are often more available in these altered environments (Cook & Blumstein, 2013).

The records of the three-toed sloth and common squirrel monkey may be related to the presence of new clusters of vegetation with the structural pattern of the primitive forest, many of which are near or intercepted by the roadway. The occasional records may be related to the potential effect that the ecological barriers roadways pose for species with tree-climbing habits (Laurance et al., 2006). However, records of roadkilled primates on Brazilian roads are not rare (Gumier-Costa & Sperber, 2009; Caceres et al., 2010; Omena-Junior et al., 2012; Costa & Dias, 2013; Machado et al., 2015; Brum et al., 2017; Corrêa et al., 2017).

The lack of significant seasonality in the roadkill records for BR 364 and other roadways (Pereira et al., 2006; Cunha et al., 2010; Costa & Dias, 2013; Silva et al., 2013; Orlandin et al., 2015) may reflect the tendency toward a predominance of species with a high capacity for adaption to varied environments. Thus, the dry and rainy seasons offer distinct resources that can be exploited by species with opportunistic generalist habits, as those occurring along BR 364. The high frequency in the rainy season is associated with the large number of records of the nine-banded armadillo, coinciding with the mating season of the species (Clevenger et al., 2003), and is probably due to the greater availability of food sources in this season (Rocha et al., 2006).

Despite the high number of roadkilled individuals, the low species diversity may be explained by the characteristics of the roadway, which favors species with a more generalist habitat and diet (González-Suárez et al., 2018). Specialist and larger mammals may avoid human environments, such as roads. Moreover, the low diversity of large mammals may stem from the reduction in natural environments (Newmark, 1996; Coffin, 2007) as well as secondary impacts of poaching in areas occupied by humans (Laurance et al., 2006). Therefore, the high degree of habitat fragmentation in Rondônia may have a negative impact on the diversity of mammals through one or a combination of factors.

The high index of roadkilled mammals in the Pampa and Atlantic Forest eco-regions may be related to greater number of roads that cross conservation units (Bager et al., 2015) or the greater number of species that occur in larger concentrations in areas near roads. This process may be related to the availability of food sources, reproductive behavior or a greater frequency of travelling along the road by species with a large living area (Cunha et al., 2015).

The higher incidence of roadkilled mammals may be attributed to biomes with greater species diversity (hotspots) (Myers et al., 2000). Moreover, the number of roadkilled individuals and species may not be only related to eco-regions, but also to the roadway systems that pass through these biomes, with heavy traffic flow crossing highly populated regions in the coastal zone of Brazil. According to Coffin et al. (2007), the conversion of forests for the establishment of rural areas in regions with a low population density in Belize is more common in areas with better soil quality and easier access. Thus, the greater records of roadkills may be associated with converted areas of quality that are closer to roadways.

The comparative findings demonstrate that, despite the smaller number of threatened species in comparison to other eco-regions, the Pampas are also fundamental to the conservation of mammals. Large and medium-sized species use forest fragments for shelter and feeding; moreover, rare species occur in an environment that is considerably threatened by fragmentation and the replacement of natural fields with agricultural activities and grazing pastures (Espinosa et al., 2016).

One hypothesis to explain the high number of endangered species in the mammal community in the Cerrado (savanna) would be related to the structure of the biome, with its greater richness of families and species and consequently more endangered species (Caceres et al., 2010). The native vegetation may not be the preferred route for many large and medium-sized mammals in highly fragmented environments, as occurs in the Cerrado. Therefore, roadways may serve as connection routes between populations among forest areas and the courses of rivers in an eco-region dominated by agriculture and grazing pastures, as observed in the Cerrado as well as a seriously threatened eco-region, such as the Atlantic Forest, which are part of the biodiversity hotspots for conservation priorities (Myers et al., 2000).

There is a need to understand the effects of roadways on the conservation of biodiversity and the challenges of integrating plans that can avoid, minimize, and compensate for the environmental impacts generated by transportation, which is an expanding sector (Bager et al., 2015).

Urgently, practical measures for avoiding and minimizing collisions with animals are fundamental to the conservation of wild fauna. More discerning environmental analyses should prioritize specific plans and projects that can minimize the impact of roadways on wild life population, especially along more vulnerable roadways and in more threatened eco-regions in Brazil.

Acknowledgements

The authorswish to express particular thanks to Júlio Dalponte for their suggestions to improve the manuscript and Rodrigo Dias for his assistance in the layout of the figures.

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Received: August 07, 2018; Accepted: October 03, 2019

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