Abstracts

Introduction

Roads have recently been recognized as an important cause of habitat fragmentation and wildlife decline around the world (Coffin 2007COFFIN, A.W. 2007. From roadkill to road ecology: A review of the ecological effects of roads. J. Transp. Geogr. 15:396-406, 10.1016/j.jtrangeo.2006.11.006.
https://doi.org/10.1016/j.jtrangeo.2006.... ). The construction of a new road or highway across a preserved landscape has direct and indirect impacts on local wildlife (Sherewood et al. 2002SHERWOOD, B., CUTLER, D. & BURTON, J. 2002. Wildlife and Roads: The Ecological Impact. Imperial College Press, London.). Roads may induce direct mortality to wildlife through collisions with vehicles, create barriers to animal movement and consequently isolate populations, produce edge effects, alter animal behavior and reproductive ability, disrupt water supplies to and from wetlands, or intensify the toxic contamination and pollution of habitats alongside roads (Andrews 1990ANDREWS, A. 1990. Fragmentation of habitat by roads and utility corridor: A review. Aust. Zool. 26:130-141, 10.7882/AZ.1990.005.
https://doi.org/10.7882/AZ.1990.005... , Spelleberg 1998, Lodé 2000LODÉ, T. 2000. Effect of a motorway on mortality and isolation of wildlife populations. Ambio 29:163-166, 10.1579/0044-7447-29.3.163.
https://doi.org/10.1579/0044-7447-29.3.1... , Trombulak & Frissel 2000). In addition, the creation or enlargement of roads may damage natural environments by creating new road cuttings and embankments that scar the landscape, increase traffic noise, and increase road lighting (Sherewood et al. 2002SHERWOOD, B., CUTLER, D. & BURTON, J. 2002. Wildlife and Roads: The Ecological Impact. Imperial College Press, London.; Forman et al. 2003FORMAN, R.T.T., SPERLING, D., BISSONETTE, J.A., CLEVENGER, A.P., CUTSHALL, C.D. & DALE, V.H. 2003. Road ecology: science and solutions. Island Press, Washington, DC.).

Because of these threats, a number of recent studies on road ecology have been conducted, especially in Europe, the United States, and Australia (Coffin 2007COFFIN, A.W. 2007. From roadkill to road ecology: A review of the ecological effects of roads. J. Transp. Geogr. 15:396-406, 10.1016/j.jtrangeo.2006.11.006.
https://doi.org/10.1016/j.jtrangeo.2006.... ). These studies have emphasized the need to plan road systems and have indicated that conservation should be a major goal of road planning (Forman et al. 2003FORMAN, R.T.T., SPERLING, D., BISSONETTE, J.A., CLEVENGER, A.P., CUTSHALL, C.D. & DALE, V.H. 2003. Road ecology: science and solutions. Island Press, Washington, DC.). In spite of the great influence of roads on the dynamics of wildlife populations, most studies examined their effects only on specific groups, such as amphibians (Hels & Buchwald 2001HELS, T. & BUCHWALD, E. 2001. The effect of road kills on amphibian populations. Biol. Conserv. 99:331-340, 10.1016/S0006-3207(00)00215-9.
https://doi.org/10.1016/S0006-3207(00)00... ), birds (Reijnen et al. 1995REIJNEN, R., FOPPEN, R., BRAAK, C.T. & THISSEN, J. 1995. The effects of car traffic on breeding bird populations in woodland. III. Reduction of density in relation to the proximity of main roads. J. Appl. Ecol. 32:187-202.), mammals (Meunier et al. 1999MEUNIER, F.D., CORBIN, J., VERHEYDEN, C. & OUVENTINP, J. 1999. Effects of landscape type and extensive management on use of motorway road sides by small mammals. Can. J. Zool. 77:108-117, 10.1139/z98-203.
https://doi.org/10.1139/z98-203... ), or reptiles (Hartmann et al. 2011HARTMANN, P.A., HARTMANN, M.T. & MARTINS, M. 2011. Snake road mortality in a protected area in the Atlantic Forest of Southeastern Brazil. South Am. J. Herpetol. 6:35-42, 10.2994/057.006.0105.
https://doi.org/10.2994/057.006.0105... ), or even individual species, such as the Iberian lynx (Felis pardina) (Ferreras et al. 1992FERRERAS, P., ALDAMA, J.J., BELTRÁN, J.F. & DELIBES, M. 1992. Rates and causes of mortality in a fragmented population of Iberian lynx Felis pardina (Temminck). Biol. Conserv. 61:197-202, 10.1016/0006-3207(92)91116-A.
https://doi.org/10.1016/0006-3207(92)911... FISCHER, W.A., RAMOS-NETO, M.B., SILVEIRA, L. & JACOMO, A.T. 2004. Human transportation network as ecological barrier for wildlife on Brazilian Pantanal-Cerrado corridors. In Proceedings of the 2003 International Conference on Ecology and Transportation (C.L. Irwin, P. Garrett, K.P. McDermott, eds). Center for Transportation and the Environment, North Carolina State University, p. 182-194.), the eastern barred bandicoot (Perameles gunnii) (Mallick et al. 1998MALLICK, S.A., HOCKING, G.J. & DRIESSEN, M.M. 1998. Road kills of the eastern barred bandicoot (Perameles gunnii) in Tasmania: an index of abun- dance. Wildlife Res. 25:139-145, 10.1071/WR96119.
https://doi.org/10.1071/WR96119... ) or the Mediterranean snake (Hierophis viridiflavus) (Capula et al. 2014CAPULA, M., RUGIERO, L., CAPIZZI, D., MILANA, G., VIGNOLI, L., FRANCO, D., PETROZZI, F. & LUISELLI, L. 2014. Long-term, climate change-related shifts in monthly patterns of roadkilled Mediterranean snakes (Hierophis viridiflavus). Herpetol. J. 24:97-102.). A few studies have dealt with the impact of roads on the local vertebrate community, describing the species that are susceptible to road mortality and identifying those whose conservation status may be threatened by roads (Yanes et al. 1995YANES, M., VELASCO, J.M. & SUÁREZ, F. 1995. Permeability of roads and railways to vertebrates: The importance of culverts. Biol. Conserv. 71:217-222, 10.1016/0006-3207(94)00028-O.
https://doi.org/10.1016/0006-3207(94)000... , Lodé 2000LODÉ, T. 2000. Effect of a motorway on mortality and isolation of wildlife populations. Ambio 29:163-166, 10.1579/0044-7447-29.3.163.
https://doi.org/10.1579/0044-7447-29.3.1... , Dodd et al. 2004DODD JUNIOR, C.K., BARICHIVICH, W.J. & SMITH, L.L. 2004. Effectiveness of a barrier wall and culverts in reducing wildlife mortality on a heavily traveled highway in Florida. Biol. Conserv. 118:619-631, 10.1016/j.biocon.2003.10.011.
https://doi.org/10.1016/j.biocon.2003.10... , Boitet & Mead, 2014BOITET, E.R. & MEAD, A.J. 2014. Application of GIS to a Baseline Survey of Vertebrate Roadkills in Baldwin County, Georgia. Southeast. Nat. 13(1):176-190.).

The effects of roads may be more severe in protected areas (Coelho et al. 2008COELHO, I.P., KINDEL, A. & COELHO, A.V.P. 2008. Roadkills of vertebrate species on two highways through the Atlantic Forest Biosphere Reserve, southern Brazil. Eur. J. Wildlife Res. 54:689-699, 10.1007/s10344-008-0197-4.
https://doi.org/10.1007/s10344-008-0197-... ). A protected area is defined as an area of land that is especially dedicated to the protection and maintenance of biological diversity and that is designated and managed to achieve specific conservation goals. The effectiveness of a protected area depends on conservation of biodiversity not only within the park or reserve but also in its vicinity (Chape et al. 2005CHAPE, S., HARRISON, J., SPALDING, M. & LYSENKO, I. 2005. Measuring the extent and effectiveness of protected areas as an indicator for meeting global biodiversity targets. Philos. Trans. R. Soc. Lond. B Biol. Sci. 360:443-55, 10.1098/rstb.2004.1592.
https://doi.org/10.1098/rstb.2004.1592... , West et al. 2006WEST, P., IGOE, J. & BROCKINGTON, D. 2006. Parks and peoples: The social impact of protected areas. Annu. Rev. Anthropol. 35:251-277.). In Brazil, most protected areas are crossed by roads or highways, or have transportation infrastructure at or close to their borders, such as Iguaçu National Park (Paraná State, 185.262,20 ha), Emas National Park (Goiás State, 131.800 ha), and Águas Emendadas Ecological Station (Distrito Federal, 10,400 ha), so they experience the previously described effects of roads (Cândido Jr. et al. 2002CÂNDIDO JUNIOR, J.F., MARGARIDO, V.P., PEGORARO, J.L., D'AMICO, A.R., MADEIRA, W.D., CASALE, V.C. & ANDRADE, L. 2002. Animais atropelados na rodovia que margeia o Parque Nacional do Iguaçu, Paraná, Brasil, e seu aproveitamento para estudos da biologia da conservação. In: III. Congresso Brasileiro de Unidades de Conservação (ed.) Anais do III congresso brasileiro de unidades de conservação. p 553., Rodrigues et al. 2002RODRIGUES, F.H.G., HASS, A., REZENDE, L.M., PEREIRA, C.S., FIGUEIREDO, C.F., LEITE, B.F. & FRANÇA, F.G.R. 2002. Impacto de rodovias sobre a fauna da estação ecológica de águas emendadas. In III Congresso Brasileiro de Unidades de Conservação (ed.) Anais do III congresso brasileiro de unidades de conservação, p. 585., Lima & Obara 2004LIMA, S.F. & OBARA, A.T. 2004. Levantamento de animais silvestres atropelados na br-277 ès margens do Parque Nacional do Iguaçu: Subsídios ao programa multidisciplinar de proteção a fauna. In VII Semana de Artes, IV Mostra do Museu Dinâmico Interdisciplinar, II Mostra Integrada de Ensino, Pesquisa e Extensão e V Simpósio da APADEC, p. 1-7., Coelho et al. 2008COELHO, I.P., KINDEL, A. & COELHO, A.V.P. 2008. Roadkills of vertebrate species on two highways through the Atlantic Forest Biosphere Reserve, southern Brazil. Eur. J. Wildlife Res. 54:689-699, 10.1007/s10344-008-0197-4.
https://doi.org/10.1007/s10344-008-0197-... ). Brazil's road network extends over 1,713,885 km and is expected to increase due to new government incentives (PAC II - Brasil 2010BRASIL 2010. Presidência da República; Ministério do Planejamento, Orçamento e Gestão. PAC: Programa de Aceleração do Crescimento. Brasília. https://www.pac.gov.br/.
https://www.pac.gov.br/... ). New studies should be conducted to determine the impact of these new roads on the Brazilian fauna, particularly in protected areas. In this article we investigate roads as a cause of vertebrate mortality in the Chapada dos Veadeiros National Park, located in Central Brazil, and address the composition, seasonal patterns, and influence of environment on wildlife mortality due to roads.

Materials and Methods

1. The study area

The study was conducted in Central Brazil, in the state of Goiás (GO), on two roads that border the Chapada dos Veadeiros National Park (CVNP) (13°51'S to 14°10'S, and 47°25'W to 47°42'W). The main road, GO 239, runs between Alto Paraíso and Colinas and comprises 72 km (22 km of paved and 50 km of unpaved road). It provides the main access to the official gate of the CVNP, located in São Jorge village (Figure 1). Additional data was obtained from highway BR 010, which runs between Alto Paraíso and Teresina de Goiás and includes 64 km of paved road. The CVPN covers approximately 65,512 ha of relatively undisturbed Cerrado. It is located in a mountainous region, the Planalto Central Goiano (Felfili et al. 2007FELFILI, J.M., REZENDE, A.V. & SILVA JUNIOR, M.C. 2007. Biogeografia do Bioma Cerrado: Vegetação e Solos da Chapada dos Veadeiros. Editora Universidade de Brasília, Finatec, Brasília.), which has altitudes ranging between approximately 620 m and 1,700 m and includes Central Brazil's highest peak (Pouso Alto, 1,784 m). The climate is type Aw in the Köppen classification, receiving annually 1500-1750 mm of a highly predictable and strongly seasonal precipitation, restricted almost entirely to October-March (Nimer 1989NIMER, E. 1989. Climatologia do Brasil. 2 ed. IBGE, Rio de Janeiro.). Long-term climatic data from the Chapada dos Veadeiros region are summarized in Figure 2. Average temperatures vary between 20°C and 26°C (Silva et al. 2001SILVA, S.R., SILVA, A.P., MUNHOZ, C.B., SILVA JUNIOR, M.C. & MEDEIROS, M.B. 2001. Guia de Plantas do Cerrado Utilizadas na Chapada dos Veadeiros. WWF-Brasil, Brasília.). The vegetation is characterized by a predominance of gallery forest formations at low elevations and Cerrado with montane savannas at high elevations (Felfili et al. 2007FELFILI, J.M., REZENDE, A.V. & SILVA JUNIOR, M.C. 2007. Biogeografia do Bioma Cerrado: Vegetação e Solos da Chapada dos Veadeiros. Editora Universidade de Brasília, Finatec, Brasília.).

2. Impact of roads

Roads as a cause of vertebrate mortality were investigated through surveys of animals killed by vehicles and by recording dead vertebrates observed on both roads on non-consecutive days, between November 2006 to April 2008. Road surveys were undertaken once every three days. The surveys were conducted by driving at 25-50 km h^-1 along GO 239 and at 60-80 km h^-1 along BR 010. When a dead animal was spotted, we stopped the car for closer inspection, identified the animal to the lowest taxonomic level possible, recorded the location with GPS, and removed the carcass from the road. Carcasses in good condition were preserved and added to the vertebrate collections of Universidade de Brasília.

The frequency of roadkill was calculated by dividing the number of individuals killed by the number of kilometers covered. The average frequencies of animals and species killed were compared between the dry season (April to September) and the rainy season (October to March). A paired t-test was used to evaluate the difference between dry and rainy seasons. Multiple regression was used to evaluate whether an association existed among roadkill, precipitation, and the structure of nearby vegetation.

3. Estimates

We constructed a species accumulation curve for all road-killed species and for each taxonomic class found on the road, using the individual-based rarefaction method (with the nonparametric Mao Tau estimator and with 95% confidence intervals) (Gotelli & Colwell 2001GOTELLI, N. & COLWELL, R.K. 2001. Quantifying biodiversity: Procedures and pitfalls in the measurement and comparison of species richness. Ecol. Lett. 4:379-391, 10.1046/j.1461-0248.2001.00230.x.
https://doi.org/10.1046/j.1461-0248.2001... ). The function of richness (Mao Tau) was computed as the accumulation function of individuals of each species. Species richness estimators were computed using nonparametric incidence-based estimators (Bootstrap, Chao 2, ICE, Jacknife 1 and 2) and abundance-based estimators (ACE and Chao 1) (Colwell & Coddington 1994COLWELL, R.K. & CODDINGTON, J.A. 1994. Estimating terrestrial biodiversity through extrapolation. Philos. T. Roy. Soc. B. 345:101-118, 10.1098/rstb.1994.0091.
https://doi.org/10.1098/rstb.1994.0091... , Colwell 2011COLWELL, R.K. 2011. EstimateS. version 8.2.0: Statistical Estimation of Species Richness and Shared Species from Samples (Software and User's Guide). Freeware for Windows and Mac OS.). Both species accumulation curve and species richness estimators were performed to evaluate the sampling effort, allowing a better comparison among the groups of vertebrates found and pointing out which groups are underestimated through the method. Species rarefaction and richness estimators were performed with Estimates 8.2.0 software.

4. Correlation of landscape with roadkill

The attributes of landscapes near roads were assessed at 1 km intervals along the entire extent of the roads, both in the preserve and in the adjacent environment, using a 1:25000 topographic map. Landscape categories were assigned according to the proportions of environmental variables contained within 50 m on both sides of the the road shoulders on each kilometer. The categories included cerrado, grassland, forest, and pasture. In addition, the presence or absence of watercourses and the presence of paved or unpaved roads surfaces were recorded at the same intervals.

To examine the relationship between road-killed vertebrates and the road landscape, we performed a Canonical Correspondence Analysis (CCA; Ter Braak 1986TER BRAAK, C.J.F. 1986. Canonical correspondence analysis: a new eigenvector technique for multivariate direct gradient analysis. Ecology 67:1167-1179, 10.2307/1938672.
https://doi.org/10.2307/1938672... ), associating variation in one matrix (vertebrate abundance as the dependent variable) with variation in another matrix (landscape characteristics as the independent variable). In this analysis, we investigated whether a connection existed between specific habitat characteristics and the abundance of particular vertebrate groups. CCA was performed with CANOCO 4.5 (Ter Braak & Smilauer 1998TER BRAAK, C.J.F. & SMILAUER, P. 1998. CANOCO: Reference Manual and User's Guide to Canoco for Windows: Software for Canonical Community Ordination (version 4). Microcomputer Power, Ithaca, NY.), using the following options: focus scaling set on symmetric, biplot scaling type, downweighting of rare species, Monte Carlo test with 1,000 permutations of the reduced model, and unrestricted permutations.

Results

A total of 260 surveys of road-killed animals were conducted in 10,658 km: 212 on GO 239 (covering 7,463 km) and 48 on BR 010 (covering 3,195 km). In all, 824 vertebrates of 138 species were recorded along the two roads (Table 1). The most commonly road-killed species for each group of vertebrates were the yellow-toothed cavy (Galea flavidens) (10.2% of total vertebrate casualties), the marbled lancehead (Bothrops marmoratus) (7.5%), the Schneider's toad (Rhinella schneideri) (5.2%), and the grassland sparrow (Ammodramus humeralis) (3.0%). Six species that are nationally listed as threatened (MMA 2008) were found: black-masked finch (Coryphaspiza melanotis, n=1, 0.12% of total vertebrate casualties), sharp-tailed tyrant (Culicivora caudacuta, n=1, 0.12%), maned wolf (Chrysocyon brachyurus, n=7, 0.84%), cougar (Puma concolor, n=1,0.12%), ocelot (Leopardus pardalis, n=3,0.36%), and giant anteater (Myrmecophaga tridactyla, n=1, 0.12%). The overall number of road-killed vertebrates in relation to road length was 0.096 animals km^-1; the overall roadkill incidence-interval was 10.42 km per roadkill. Reptiles were the most frequently killed group on both roads, followed by birds, mammals, and amphibians (Table 2).

Vertebrate mortality was significantly higher during the wet season than during the dry season (paired t-test, t=4.935, df=285, P < 0.000) and mortality differed between the two seasons for all taxonomic groups: amphibians (paired t-test, t=−2.576, df=23, P=0.017), birds (paired t-test, t=−3.184, df=125, P=0.002), mammals (paired t-test, t=−2.854, df=45, P=0.007) and reptiles (paired t-test, t=−2.141, df=89, P=0.035). In addition, a stepwise multiple regression analysis showed that there was no association between vertebrate roadkill and precipitation (r=0.489; F=3.138;P=0.107).

Species rarefaction curves did not reach stability (Figure 3). The species richness estimators produced estimates greater than the actual recorded species richness for all taxonomic groups (Table 3). The major estimates with the major standard deviations were recorded with Chao 1 and 2 and the minor estimates were recorded with Bootstrap estimator (Table 3).

A summary of road and landscape attributes appears in Table 4. On the basis of 9,999 permutations of a Monte Carlo test and the first canonical axis, we found a significant relationship between habitat structure within arrays and vertebrate groups found there (eigenvalue=0.146, F_4,35=14.958, P < 0.001). In addition, all canonical axes were significant (trace=0.205, F_4,35=4.444, P < 0.001). Amphibians were associated with nearby forest and paved roads, birds were associated with nearby pasture, reptiles were associated with nearby grassland, and mammals were associated with unpaved road (Figure 4).

Discussion

The high number of road-killed vertebrates in CVNP indicates that the roads surrounding the park may significantly affect the wild vertebrates populations. The species richness found in our study (138 species) was greater than that reported by other long-term studies of Brazilian roads or motorways. Coelho et al. (2008)COELHO, I.P., KINDEL, A. & COELHO, A.V.P. 2008. Roadkills of vertebrate species on two highways through the Atlantic Forest Biosphere Reserve, southern Brazil. Eur. J. Wildlife Res. 54:689-699, 10.1007/s10344-008-0197-4.
https://doi.org/10.1007/s10344-008-0197-... recorded 92 species on two roads in the northern coastal plain of Rio Grande do Sul; Rodrigues et al. (2002)RODRIGUES, F.H.G., HASS, A., REZENDE, L.M., PEREIRA, C.S., FIGUEIREDO, C.F., LEITE, B.F. & FRANÇA, F.G.R. 2002. Impacto de rodovias sobre a fauna da estação ecológica de águas emendadas. In III Congresso Brasileiro de Unidades de Conservação (ed.) Anais do III congresso brasileiro de unidades de conservação, p. 585. found 100 species on four roads that delimit Águas Emendadas Ecological Station, in Distrito Federal; and Prada (2004)PRADA, C.S. 2004. Atropelamento de vertebrados silvestres em uma região fragmentada no nordeste no estado de São Paulo: quantificação do impacto e análise de fatores envolvidos. Dissertação de mestrado, Universidade Federal de São Carlos, São Carlos. found 83 species on six roads in northeastern São Paulo. Fisher et al. (2003) recorded 140 species of vertebrates on BR 262, in the Pantanal wetlands of Mato Grosso do Sul, over the course of an 8-year-long study. The road mortality around CVNP is also high in comparison with other areas worldwide, such as Australia (Taylor & Goldingay 2004TAYLOR, B.D. & GOLDINGAY, R.L. 2004. Wildlife road-kills on three major roads in north-eastern New South Wales. Wildlife Res. 31(1):83-91, 10.1071/WR01110.
https://doi.org/10.1071/WR01110... , n=53), Europe (Lodé 2000LODÉ, T. 2000. Effect of a motorway on mortality and isolation of wildlife populations. Ambio 29:163-166, 10.1579/0044-7447-29.3.163.
https://doi.org/10.1579/0044-7447-29.3.1... , n=97), and North America (Ashley and Robinson 1996ASHLEY, E.P. & ROBINSON, J.T. 1996. Road mortality of amphibians, reptiles and other wildlife on the Long Point causeway, Lake Erie, Ontario. Can. Field Nat. 110:403-412., n=100). However, the overall number of 0.096 road-killed vertebrates per kilometer was similar to that of other studies in Brazil, ranging from 0.078 animals km^-1 on BR-383, in Rondônia (Turci & Bernarde 2009), to 0.138 on BR-307, in Acre (Pinheiro & Turci 2013PINHEIRO, B.F. & TURCI, L.C. 2013. Vertebrados atropelados na estrada da Variante (BR-307), Cruzeiro do Sul, Acre, Brasil. Natureza on line. 11(2):68-78.).

Despite the high number of vertebrates found during our surveys, the results are still an underestimate of total roadkill. The survey method of the present study (searches by car) allows the record of many roadkills, but due to the car speed it may overlook small animals, such as small amphibians and birds (Coelho et al. 2008COELHO, I.P., KINDEL, A. & COELHO, A.V.P. 2008. Roadkills of vertebrate species on two highways through the Atlantic Forest Biosphere Reserve, southern Brazil. Eur. J. Wildlife Res. 54:689-699, 10.1007/s10344-008-0197-4.
https://doi.org/10.1007/s10344-008-0197-... ). Besides, by not searching the roads constantly (more than twice a day, for example), some animals are not recorded because they quickly disappear. For instance, scavenging predators could have removed numerous small dead animals from the roads (Antworth et al. 2005ANTWORTH, R.L., PIKE, D.A. & STEVENS, E.E. 2005. Hit and Run: Effects of Scavenging on Estimates of Roadkilled Vertebrates. Southeast. Nat. 4(4):647-656, 10.1656/1528-7092(2005)004[0647:HAREOS]2.0.CO;2.
https://doi.org/10.1656/1528-7092(2005)0... ). In addition, some animals may have been thrown away from the road by the collision or may have been only wounded by the collision and died far from the road (Slater 2002SLATER, F.M. 2002. An assessment of wildlife road casualties - the potential discrepancy between numbers counted and numbers killed. Web Ecol. 3:33-42, 10.5194/we-3-33-2002.
https://doi.org/10.5194/we-3-33-2002... ). Nevertheless, the method of search by car permits the inspection of a great road extension in a short amount of time and it is comparable to similar surveys. Rarefaction curves for all groups do not reach stability, a common trend in roadkill studies (Santana 2009, Pinheiro & Turci 2013PINHEIRO, B.F. & TURCI, L.C. 2013. Vertebrados atropelados na estrada da Variante (BR-307), Cruzeiro do Sul, Acre, Brasil. Natureza on line. 11(2):68-78.). Estimates also show that a high number of species for all groups are affected by the roads in CVNP. For example, at least 47 species of snake inhabit the park (França & Braz 2013FRANÇA, F.G.R. & BRAZ, V.S. 2013. Diversity, activity patterns, and habitat use of the snake fauna of Chapada dos Veadeiros National Park in Central Brazil. Biota Neotropica, 13(1): http://www.biotaneotropica.org.br/v13n1/pt/abstract?article+bn01313012013.
http://www.biotaneotropica.org.br/v13n1/... ), of which we found only 37 on the roads. Some species that are common in the Cerrado and that have been found in previous studies are the brown-banded water snake (Helicops angulatus), the southern crested caracara (Caracara plancus), the American black vulture (Coragyps atratus), the greater grison (Galictis vittata), and the nine-banded armadillo (Dasypus novemcinctus). These species will probably appear in future surveys of roads around the CVNP.

Among the four vertebrate classes found as roadkill, the impact on amphibians is most likely to have been underestimated, due to their small size, their thin skin, and the slow locomotion of many amphibian species. The carcasses do not last as long on roads as those of other vertebrates because scavengers eat them rapidly or they are run over many times and are rapidly obliterated by vehicles (Hels & Buchwald 2001HELS, T. & BUCHWALD, E. 2001. The effect of road kills on amphibian populations. Biol. Conserv. 99:331-340, 10.1016/S0006-3207(00)00215-9.
https://doi.org/10.1016/S0006-3207(00)00... ). Also, due to their activity patterns, seasonal reproduction, population structure, and selected habitats, amphibians are commonly more vulnerable to being hit by vehicles than other species (Hels & Buchwald 2001HELS, T. & BUCHWALD, E. 2001. The effect of road kills on amphibian populations. Biol. Conserv. 99:331-340, 10.1016/S0006-3207(00)00215-9.
https://doi.org/10.1016/S0006-3207(00)00... ). Most data regarding road-killed amphibians are for large toads and frogs of the Bufonidae and Leptodactylidae families, the carcasses of which remain longer on the roads (Fahrig et al. 1995FAHRIG, L., PEDLAR, J.H., POPE, S.E., TAYLOR, P.D. & WEGNER, J.F. 1995. Effects of road traffic on amphibian density. Biol. Conserv. 73:177-182, 10.1016/0006-3207(94)00102-V.
https://doi.org/10.1016/0006-3207(94)001... ). The most commonly found amphibian in our surveys, the Schneider's toad (Rhinella schneideri), is a very common species in the Brazilian Cerrado, and individuals belonging to the genus Rhinella are often found as roadkill in different regions, such as Amazonia and the Atlantic Forest (Silva et al. 2007SILVA, M.O., OLIVEIRA, I.S., CARDOSO, M.W. & GRAF, V. 2007. Impacto dos atropelamentos sobre a herpetofauna da Floresta Atlântica (PR-340, Antonina, Paraná). Acta Biol. Paran. 36:103-112, 10.5380/abpr.v36i0.9668.
https://doi.org/10.5380/abpr.v36i0.9668... , Turci & Bernarde 2009).

Birds are also likely underestimated, particularly small passerines. Usually birds are hit while they are in flight and are thrown off the roads by the impact (Erritzoe et al. 2003ERRITZOE, J., MAZGAJSKI, T. & REJT, Ł. 2003. Bird casualties on European roads—a review. Acta Ornithol. 38:77-93, 10.3161/068.038.0204.
https://doi.org/10.3161/068.038.0204... ). Many hawks and buzzards are hit while scavenging roadkill (Antworth et al. 2005ANTWORTH, R.L., PIKE, D.A. & STEVENS, E.E. 2005. Hit and Run: Effects of Scavenging on Estimates of Roadkilled Vertebrates. Southeast. Nat. 4(4):647-656, 10.1656/1528-7092(2005)004[0647:HAREOS]2.0.CO;2.
https://doi.org/10.1656/1528-7092(2005)0... ). In addition, the type of habitat near roads can attract birds to the roads and increase their risk of becoming roadkill. For example, many small birds move and forage in the vegetation along the roads (Orłowski 2005ORŁOWSKI, G. 2005. Factors affecting road mortality of barn swallow Hirundo rustica in farmland. Acta Ornithol. 40:117-125, 10.3161/068.040.0207.
https://doi.org/10.3161/068.040.0207... ). In natural landscapes crossed by roads, the roadside vegetation serves as a corridor and ecotone used by insects and birds, facilitating movement and feeding along the border of an area, but birds that spend time in this area are at higher risk of being hit by vehicles (Orłowski 2008ORŁOWSKI, G. 2008. Roadside hedgerows and trees as factors increasing road mortality of birds: Implications for management of roadside vegetation in rural landscapes. Landscape Urban Plan. 86:153-161, 10.1016/j.landurbplan.2008.02.003.
https://doi.org/10.1016/j.landurbplan.20... , Rosa & Badger 2012). Most road-killed birds in the CVNP were species that use road borders frequently, such as the grassland sparrow (Ammodramus humeralis) and the blue-black grassquit (Volatinia jacarina). Although some authors have described roadkill as having low influence on the population dynamics of birds (Reijnen et al. 1995REIJNEN, R., FOPPEN, R., BRAAK, C.T. & THISSEN, J. 1995. The effects of car traffic on breeding bird populations in woodland. III. Reduction of density in relation to the proximity of main roads. J. Appl. Ecol. 32:187-202.), these impacts can be proportionally greater in threatened species, such as certain grassland birds in the Cerrado, like the black-masked finch (Coryphaspiza melanotis). This species should receive special attention and mitigation programs, because it is nationally threatened species in Brazil (Brazilian National list of endangered species Portaria MMA no 444/2014).

Mammals are usually affected by roads when they have wide home ranges and terrestrial habits, which make them use roads as corridors for movement (Smith-Patten & Patten 2008SMITH-PATTEN, B.D. & PATTEN, M.A. 2008. Diversity, Seasonality, and Context of Mammalian Roadkills in the Southern Great Plains. Environ. Manage. 41(6):844-852. SPELLERBERG, I.F. 1998. Ecological effects of roads and traffic: A literature review. Global Ecol. Biogeogr. 7:317-333, 10.1046/j.1466-822x.1998.00308.x.
https://doi.org/10.1046/j.1466-822x.1998... SHERWOOD, B., CUTLER, D. & BURTON, J. 2002. Wildlife and Roads: The Ecological Impact. Imperial College Press, London.). Also, many mammals are nocturnal and/or are scavengers. At night, they are targets for vehicles because they can become blind and immobilized on roads when cars' headlights shine on them (Barthelmess & Brooks 2010BARTHELMESS, E.L. & BROOKS, M.S. 2010. The influence of body-size and diet on road-kill trends in mammals. Biodivers. Conserv. 19:1611-1629, 10.1007/s10531-010-9791-3.
https://doi.org/10.1007/s10531-010-9791-... ). Both the hoary fox (Lycalopex vetulus) and the crab-eating fox (Cerdocyon thous) are commonly hit by cars for this reason. These omnivorous, nocturnal and generalist foxes have ample distributions in South America and abundant populations (Wozencraft 2005WOZENCRAFT, W.C. 2005. Order Carnivora. In Mammal Species of the World (D.E. Wilson & D.M. Reeder, eds.). 3 ed. Johns Hopkins University Press, Baltimore, p. 532-628.) and are frequently found on various roads (Vieira 1996VIEIRA, E.M. 1996. Highway mortality of mammals in Central Brazil. Cienc. Cult. 48:270-272., Silveira 1999SILVEIRA, L. 1999. Ecologia e conservação dos mamíferos carnívoros do Parque Nacional das Emas. Dissertação de mestrado, Universidade Federal de Goiás, Goiânia., Coelho 2003, Prada 2004PRADA, C.S. 2004. Atropelamento de vertebrados silvestres em uma região fragmentada no nordeste no estado de São Paulo: quantificação do impacto e análise de fatores envolvidos. Dissertação de mestrado, Universidade Federal de São Carlos, São Carlos.). Another small mammal that was frequently found on CVNP roads was the yellow-toothed cavy (Galea flavidens). Despite its high abundance in the CVPN, this species is not common, as it is endemic to Brazil and restricted to the montane savanna habitat (Bonvincino et al. 2005, Weksler & Bonvicino 2008WEKSLER, M. & BONVICINO, C. 2008. Galea flavidens. In 2008 IUCN Red List of Threatened Species. http://www.iucnredlist.org.
http://www.iucnredlist.org... ). Finally, other mammals that require special conservation attention are the giant anteater (Myrmecophaga tridactyla), the cougar (Puma concolor), and the maned wolf (Chrysocyon brachyurus). These are Brazilian threatened species and their populations are low in Central Brazil (Brazilian National list of endangered species Portaria MMA no 444/2014).

Snakes are the reptiles that are most likely to be hit on roads, due to their characteristic long body morphology and their habit of frequently using roads as thermoregulation sites (Bernardino & Dalrymple 1992BERNARDINO JUNIOR, F.S. & DALRYMPLE, G.H. 1992. Seasonal activity and road mortality of the snakes of the pa-hay-okee wetlands of Everglades National Park, USA. Biol. Conserv. 62:71-75, 10.1016/0006-3207(92)90928-G.
https://doi.org/10.1016/0006-3207(92)909... , Bonnet et al. 1999BONNET, X., NAULLEAU, G. & SHINE, R. 1999. The dangers of leaving home: dispersal and mortality in snakes. Biol. Conserv. 89:39-50, 10.1016/S0006-3207(98)00140-2.
https://doi.org/10.1016/S0006-3207(98)00... BONVICINO, C.R., LEMOS, B. & WEKSLER, M. 2005. Small mammals of Chapada dos Veadeiros National Park (Cerrado of central Brazil): ecology, karyologic, and taxonomic considerations. Braz. J. Biol. 65(3):1-12, 10.1590/S1519-69842005000300004.
https://doi.org/10.1590/S1519-6984200500... ). Most reptiles found on CVPN roads were snakes or long-bodied lizards, such as Ophiodes aff. striatus. Terrestrial and sit-and-wait genera, such as Bothrops, Crotalus, and Oxyrhopus, and slow-moving reptiles, such as Polychrus acutirostris and the worm lizards of the genus Amphisbaena, are commonly hit by vehicles. No reptile species are listed as threatened in Central Brazil. However, species with life histories characterized by low reproductive rates and low adult mortality, such as the Vanderhaege's toad-headed turtle (Phrynops vanderhaegei), and huge snakes and vipers, are more vulnerable to the demographic consequences of road mortality (Forman et al. 2003FORMAN, R.T.T., SPERLING, D., BISSONETTE, J.A., CLEVENGER, A.P., CUTSHALL, C.D. & DALE, V.H. 2003. Road ecology: science and solutions. Island Press, Washington, DC., Shepard 2009).

The species richness of roadkill and the roadkill rates are influenced by seasonality as well as by type of nearby habitat (Trombulak & Frissell 2000TROMBULAK, S.C. & FRISSELL, C.A. 2000. Review of ecological effects of roads on terrestrial and aquatic communities. Conserv. Biol. 14:8-30, 10.1046/j.1523-1739.2000.99084.x.
https://doi.org/10.1046/j.1523-1739.2000... , Rosa & Bager 2012ROSA, C.A. & BAGER, A. 2012. Seasonality and habitat types affect roadkill of neotropical birds. J. Environ. Manage. 97:1-5. SANTANA, S.G. 2012. Fatores influentes sobre atropelamentos de vertebrados na região central do Rio Grande do Sul, Brasil. Neotrop. Biol. Conserv. 7:26-40, 10.4013/nbc.2012.71.05.
https://doi.org/10.4013/nbc.2012.71.05... ). There are two well-defined seasons in Central Brazil, the wet or rainy season, characterized by high precipitation, and the dry season, during which almost no rain falls (Nimer 1989NIMER, E. 1989. Climatologia do Brasil. 2 ed. IBGE, Rio de Janeiro.). Vertebrate mortality on CVNP roads was significantly higher during the wet season, as reported by previous studies in Central Brazil (Rodrigues et al. 2002RODRIGUES, F.H.G., HASS, A., REZENDE, L.M., PEREIRA, C.S., FIGUEIREDO, C.F., LEITE, B.F. & FRANÇA, F.G.R. 2002. Impacto de rodovias sobre a fauna da estação ecológica de águas emendadas. In III Congresso Brasileiro de Unidades de Conservação (ed.) Anais do III congresso brasileiro de unidades de conservação, p. 585.). Studies show that more Brazilian mammals (Cáceres et al. 2012CÁCERES, N.C., CASELLA, J.E.C. & GOULART, S. 2012. Variação Espacial e Sazonal de atropelamentos de mamíferos no Bioma Cerrado, Rodovia Br 262, Sudoeste do Brasil. Mastozool. Neotrop. 19(1):21-33.) and anurans (Coelho et al. 2012COELHO, I.P., TEIXEIRA, F.Z., COLOMBO, P., COELHO A.V.P. & KINDEL, A. 2012 Anuran road-kills neighboring a peri-urban reserve in the Atlantic Forest, Brazil. J. Environ. Manage. 112:17-26.) are killed on roads during the rainy season. The Cerrado of Central Brazil shows high seasonality and the activity of vertebrates becomes more intense after the first rainfalls (Oliveira & Marquis 2002OLIVEIRA, P.S. & MARQUIS, R.J. 2002. The Cerrados of Brazil. Ecology and natural history of a neotropical savanna. Columbia University Press, New York.). Even for plants, the rainy season is a more active time; although fructification of anemochorous and autochorous species occurs during the dry season, the fructification of zoochorous species is dispersed throughout the rainy season (Batalha & Mantovani 2000BATALHA, M.A. & MANTOVANI, W. 2000. Reproductive phenological patterns of Cerrado plant species at the Pé-de-Gigante Reserve (Santa Rita do Passa Quatro, SP, Brazil): a comparison between the herbaceous and woody floras. Rev. Bras. Biol. 60(1):129-145, 10.1590/S0034-71082000000100016.
https://doi.org/10.1590/S0034-7108200000... BAGER, A. & ROSA, C.A. 2010. Hierarquização de quilômetros prioritários è mitigação de atropelamentos de animais selvagens. Biota Neotropica 10(4): http://www.biotaneotropica.org.br/v10n4/pt/abstract?article+bn03010042010.
http://www.biotaneotropica.org.br/v10n4/... ). Also, many animal species of Cerrado show dispersion and migratory movements and reproductive activities during the rainy season, when roads become barriers to their intense locomotion.

Amphibians were associated with patches of paved road with nearby forest habitat. In the Cerrado, gallery forests are always associated with streams and rivers, suitable environments for amphibians (Colli et al. 2002COLLI, G.R., BASTOS, R.P. & ARAÚJO, A.F.B. 2002. The character and dynamics of the Cerrado herpetofauna. In The Cerrados of Brazil: Ecology and Natural History of a Neotropical Savanna (P.S. Oliveira & R.J. Marquis, eds.). Columbia New York. University Press, p.223-241.). These animals are at increased risk of being hit on high-speed paved roads and are killed mainly during the reproductive season. In contrast, there were more road-killed birds along roads next to pasture habitats. Despite their preference for forest habitats, birds that live in rural landscapes are usually associated with roads that are bordered by native vegetation. These roads can be attractive habitat and potentially a population sink, and offer a higher abundance of insects than other areas, attracting birds (Orłowski 2008ORŁOWSKI, G. 2008. Roadside hedgerows and trees as factors increasing road mortality of birds: Implications for management of roadside vegetation in rural landscapes. Landscape Urban Plan. 86:153-161, 10.1016/j.landurbplan.2008.02.003.
https://doi.org/10.1016/j.landurbplan.20... ).

In contrast with amphibians and birds, most of the reptiles and small mammals of the Cerrado are associated with open areas, and the majority of snakes found in the CVNP are found in grasslands or open savanna environments (França & Braz 2013FRANÇA, F.G.R. & BRAZ, V.S. 2013. Diversity, activity patterns, and habitat use of the snake fauna of Chapada dos Veadeiros National Park in Central Brazil. Biota Neotropica, 13(1): http://www.biotaneotropica.org.br/v13n1/pt/abstract?article+bn01313012013.
http://www.biotaneotropica.org.br/v13n1/... ). Roadkilled mammals were strongly associated with unpaved road. In spite of the fact that mammals inhabit mainly forest habitats in the Cerrado (Johnson et al. 1999JOHNSON, M.A., SARAIVA, P.M. & COELHO, D. 1999. The role of gallery forests in the distribution of Cerrado mammals. Rev. Bras. Biol. 59(3):421-427.), most species have wide home ranges and may traverse the entire Cerrado. Compared with paved roads, unpaved roads appear to be more suitable and less exposed environments that enable the movements of CVNP mammals.

Due to the importance of the CVNP as a protected area that harbors and maintains the biodiversity of the Cerrado, it is important to remain monitoring the impact of the park's roads on wild vertebrates. Further studies may use recent indices and analyses to measure the impact of roads on the fauna of the CVNP and to establish priorities for mitigation programs (Coelho et al. 2008COELHO, I.P., KINDEL, A. & COELHO, A.V.P. 2008. Roadkills of vertebrate species on two highways through the Atlantic Forest Biosphere Reserve, southern Brazil. Eur. J. Wildlife Res. 54:689-699, 10.1007/s10344-008-0197-4.
https://doi.org/10.1007/s10344-008-0197-... , Bager & Rosa 2011). Some mitigation actions are urgently needed, such as highway fencing in combination with safe crossing opportunities for wildlife (Clevenger et al. 2001CLEVENGER, A.P., CHRUSZCZ, B., GUNSON, K.E. 2001. Highway mitigation fencing reduces wildlife-vehicle collisions. Wildlife Soc. Bull. 29:646-653.).

Acknowledgments

The authors are grateful to Daniel Rios de Magalhães Borges and ICMbio for collection permits in the Chapada dos Veadeiros National Park (IBAMA license 051/2007 and SISBIO license 15325-1). We thank Santos Balbino, Davi Pantoja, and Iubatã Farias for their generous help during fieldwork, Rafaela França for the map of CVNP, and José Augusto Drummond, Marcel Bursztyn, Marília Machado and Rebeca Roysen for their suggestions to improve the manuscript. We also thank the National Counsel of Technological and Scientific Development (CNPq) for a graduate scholarship and the Fundação O Boticário de Proteção è Natureza for financial support (0754_20072).

References

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