51P. Ribeiro et al. : The effect of roadkills on the persistence of xenarthran populations: the case of the Brazilian Cerrado

Edentata 18 (2017): 51–61DOI: 10.2305/IUCN.CH.2017.Edentata-18-1.7.en

Electronic version: ISSN 1852-9208 Print version: ISSN 1413-4411

http://www.xenarthrans.org

The effect of roadkills on the persistence of xenarthran populations: the case of the Brazilian Cerrado

paulo RibeiRoa,1, jeffeRson eDuaRDo silveiRa miRanDab,c anD Danielle RoDRiGues De aRaújoD

A Programa de Pós Graduação em Zoologia, Universidade Estadual de Santa Cruz – UESC, Rodovia Ilhéus–Itabuna, Salobrinho, CEP 45662-900, Ilhéus, BA, Brasil. E-mail: phpinheiro@yahoo.com.br

B Faculdade de Iporá – FAI, Rua Serra Cana Brava, Qd 02, Lt 04, N° 512 Jardim Novo Horizonte II, CEP 76200-000, Iporá, GO, Brasil. E-mail: jefferson.jesm@gmail.com

C Programa de Pós-graduação em Ecologia e Conservação, Universidade do Estado de Mato Grosso (UNEMAT), Caixa postal – 08, CEP 78690-000, Nova Xavantina, MT, Brasil

D Programa de Pós-Graduação Stricto Sensu em Recursos Naturais do Cerrado, Universidade Estadual de Goiás – UEG, Br 153 nº 3.105 – Fazenda Barreiro do Meio, Caixa Postal 459, CEP 75132-400, Anápolis, GO, Brasil. E-mail: msc.araujodr@gmail.com

¹ Corresponding author

Abstract The Brazilian Cerrado possesses a great diversity of xenarthrans with 12 species: eight armadillos, three anteaters, and one sloth. Even though several of these species are threatened, roadkill is considered a major threat only to Bradypus variegatus and a justification for listing Myrmecophaga tridactyla as Vulnerable. Here we present evidence that roadkill is a risk factor for xenarthran persistence, even to non-threatened species. To assess roadkill impact, we compiled articles related to mammal roadkill in the Brazilian Cerrado. One or more species of Xenarthra were among the top five most common roadkilled species in over 90% of the studies. The group represented over 50% of the recorded mammals in 33.3% of the papers and more than 40% in 66.6% of them. In 33.3% of the papers Pilosa contributed over 25% of the records and Cingulata presented the same proportion in 44.4% of them. This study reinforces the idea that roadkill must be consid-ered a major threat to xenarthran populations in conservation status assessments. Therefore, we suggest that mitigation measures be implemented, and that the IUCN take into account that roadkill is one of the greatest threats to populations of xenarthrans. Keywords: anthropic effect, Cingulata, conservation, Pilosa

Efeito do atropelamento na persistência dos xenarthras: o caso do Cerrado brasileiro

Resumo O Cerrado brasileiro possui uma grande diversidade de xenarthras, com 12 espécies: oito tatus, três tamanduás e uma preguiça. Ainda que várias dessas espécies sejam ameaçadas, o atropelamento é considerado uma ameaça maior apenas para Bradypus variegatus e uma justificativa para a vulnerabilidade de Myrmecophaga tridactyla. Neste estudo apresentamos evidências de que o atropelamento é um fator de risco para os xenarthras, mesmo para espécies que ainda não são consideradas ameaçadas. Para conhecer o impacto dos atropelamentos nas espécies do grupo, compilamos trabalhos sobre atropelamentos de mamí-feros no Cerrado. Xenarthras estão entre as cinco espécies mais registradas em mais de 90% dos trabalhos. O grupo representa mais de 50% dos animais registrados em 33,3% dos artigos, e mais de 40% em 66,6% dos mesmos. Em 33,3% dos artigos, Pilosa representa mais de 25% dos registros e Cingulata apresenta a mes-ma proporção em 44,4%. Esse estudo reforça a ideia de que o atropelamento tem que ser considerado uma ameaça maior em estudos que determinem estados de conservação. Sendo assim, sugerimos que medidas de mitigação sejam implantadas, mas, principalmente, IUCN leve em conta que o atropelamento é uma das maiores ameaças às populações de xenarthras. Palavras chave: Cingulata, conservação, efeito antrópico, Pilosa

52 Edentata 18: 51–61 (2017)

IntroductionHighways are one of the main causes of bio-

diversity loss (Coffin, 2007; Cáceres et al., 2010). Roadkill of wildlife seriously decreases animal pop-ulations, and can even result in local extinctions (Rosa & Mauhs, 2004; Prado et al., 2006; Bager et al., 2007). Highways interfere with the natural distri-bution of animals because they fragment habitats, which forces some species to cross roads (Rosa et al., 2012).

Biodiversity loss due to roadkill mostly occurs in fragmented landscapes (Carvalho et al., 2009), such as the Cerrado biome, one of 34 world biodi-versity hotspots that is home to a large number of rare, endemic, and threatened species (Bellard et al., 2014). The Cerrado has been heavily impacted by the agricultural technology and energy industries (Ab’Saber, 2003), and currently contains multiple highways used to transport grain (Correa & Ramos, 2010).

The Cerrado is an important study area for mam-mals because it harbors 251 species, of which 32 are endemic (Paglia et al., 2012). Furthermore, for Brazil, this biome is tied with the Atlantic Forest for having

the second highest diversity of Xenarthra (12 spe-cies), including eight members of Cingulata (arma-dillos, represented by: Euphractus sexcinctus, Dasypus novemcinctus, D. septemcinctus, Cabassous tatouay, C. unicinctus, Tolypeutes matacus, T. tricinctus, and the largest living armadillo, Priodontes maximus) and four of Pilosa (anteaters and sloths: Myrmecophaga tridactyla, Tamandua tetradactyla, Cyclopes didactylus, and Bradypus variegatus); only Amazonia (13 species) is more diverse (Paglia et al., 2012).

Fortunately, only three species (M. tridactyla, T. tricinctus, and P. maximus) of the 12 found in the Cerrado are classified as Vulnerable (IUCN, 2017). According to the IUCN Red List of Threatened Species, the most dangerous threats to xenarthran populations are hunting, fire, and habitat fragmen-tation. Of the xenarthrans occurring in the Cerrado, roadkill has been used in conservation assessments only as a justification for the status of M. tridactyla and is listed as a major threat only for B. variegatus (IUCN, 2017). However, roadkill could provide im-portant insights into the status of both threatened and not threatened species (IUCN, 2017). For ex-ample, Diniz & Brito (2015) estimated that roadkill

Figure 1. Locations of all studies utilized in this paper. Numbers are defined in Appendix 1; points represent the initial location of each study.

53P. Ribeiro et al. : The effect of roadkills on the persistence of xenarthran populations: the case of the Brazilian Cerrado

could lead M. tridactyla populations to extinction within 15 years.

The present work is a case study based on a literature review of studies about roadkills in the Cerrado. Our goal was to assess the risk of this an-thropic disturbance to the superorder Xenarthra.

Materials and MethodsWe conducted a search for literature about road-

killed terrestrial mammals in the Cerrado, including papers, theses, and book chapters, in order to tabulate the total number of roadkilled individuals for each species. We used the following platforms: Google Scholar, Scielo, and Thomson’s ISI Web of Science, using the keyword “roadkill”, associated with the terms: Xenarthra, Pilosa, Cingulata, Mammals, and Cerrado. Works were excluded if they lacked the in-formation necessary to calculate these totals. Species were grouped according to order, and the mean pro-portion of specimens per order was compared using an ANOVA, with post-hoc pair-wise comparisons using Tukey’s test. Proportions were calculated by dividing the total number of specimens for each or-der by the total number of individuals recorded in each study. The analyses were conducted using the software R (R Core Team, 2016).

ResultsWe found 36 articles, but only 18 contained the

necessary data for our analyses (absolute frequency of roadkill by species). These 18 articles included 14 peer-reviewed papers, three theses, and one book chapter (Fig. 1, Appendix 1).

Xenarthrans represented over 50% of the recorded mammals in 33.3% of the articles and more

than 40% in 66.6% of them (Fig. 2). In 33.3% of these papers Pilosa represented over 25% of records, and Cingulata presented the same proportion in 44.4% of them.

We found an overall difference in roadkill pro-portions between orders (F=7.5; df=8, 150; p<0.05). The proportion of Cingulata recorded as roadkill was significantly higher than that of Lagomorpha, Artiodactyla, and Didelphimorphia. Pilosa differed only from Lagomorpha. One or more xenarthrans were among the top five most common roadkilled species in 17 of 18 studies (Fig. 3). Euphractus sexcinc-tus was in the top five in 14 of these, M. tridactyla and T. tetradactyla in 12.

DiscussionSeveral studies of mammalian roadkill con-

ducted in other biomes found that xenarthrans were the most affected group (Prado et al., 2006; Tumeleiro et al., 2006; Cherem et al., 2007; Bueno & Almeida 2010; Hegel et al., 2012; Santana, 2012), in-dicating that this problem goes beyond the Cerrado. Therefore, statements that changes in population size caused by human activities may not be rele-vant to the conservation of xenarthrans (e.g., Shaw et al., 1987) can be ruled out. Indeed, Cáceres (2011) reported that species such as E. sexcinctus, D. novem-cinctus, C. tatouay, M. tridactyla, and T. tetradactyla are extremely prone to being run over, which suggests mortality from roadkill should be taken seriously.

Several features of xenarthrans may contrib-ute to their high incidence as roadkill. For example, most xenarthrans possess poor vision (Redford & Wetzel, 1985; Medri et al., 2011; Freitas et al., 2014), which may increase their risk of being killed while crossing roads because they do not see oncoming

Figure 2. Proportion of roadkill per mammalian order in the publications analyzed in the present study.

54 Edentata 18: 51–61 (2017)

Figure 3. Absolute frequency of the five most common roadkilled species found in each study. Xenarthrans are represented by black bars. Legend: c_bra: Chrysocyon brachyurus; c_fam: Canis familiaris; c_pac: Cuniculus paca; c_preh: Coendou prehensilis; c_semi: Conepatus semistriatus; c_thous: Cerdocyon thous; d_alb: Didelphis albiventris; d_mar: Didelphis marsupialis; d_nov: Dasypus nove-mcinctus; e_sex: Euphractus sexcinctus; f_cat: Felis catus; g_fla: Galea flavidens; h_hid: Hydrochoerus hydrochaeris; l_vet: Lycalopex vetulus; m_tri: Myrmecophaga tridactyla; n_nas: Nasua nasua; p_can: Procyon cancrivorus; s_bra: Sylvilagus brasiliensis; t_pec: Tayassu pecari; t_tetra: Tamandua tetradactyla; rod: non identified Rodentia; and NI_arm: non identified armadillo.

55P. Ribeiro et al. : The effect of roadkills on the persistence of xenarthran populations: the case of the Brazilian Cerrado

traffic soon enough to avoid a collision. In addition, species such as armadillos do not possess a tapetum lucidum, a common membrane in other mammals, such as carnivores (Ollivier et al., 2004), which assists in light capture, mainly in nocturnal animals. When illuminated by a strong light, such as car lights, the tapetum lucidum shines, which, according to Loughry & McDonough (2013), may allow drivers to avoid hitting animals on the road. Because armadillos do not possess this membrane, spotting them on roads during the night is harder. This, coupled with their relatively small body size, may explain why arma-dillos are found so commonly as roadkills.

The silky anteater (C. didactylus) has a hearing frequency range of 0.6–62 Hz (Hayssen et al., 2012), which is below the minimum frequency produced by tires and diesel engine vehicles (200–700 Hz). Thus, this species may be vulnerable to roadkill mortality because it fails to hear the approach of on-coming traffic.

Sloths are notoriously slow animals, in part due to their low metabolism, which might seem to put them at great risk for roadkill. However, sloths rarely move to the ground (Hayssen, 2010) which probably explains the low incidence of this species in roadkill studies.

Finally, the anatomy of xenarthrans does not make them very agile. Specifically, plantigrade lo-comotion, coupled with short limbs, provides low agility and relatively slow locomotion.

Carnivora also presents a high incidence of roadkills, in some cases higher than Xenarthra. This is mostly due to the great number of crab-eating foxes (Cerdocyon thous) that were found. This species occurs at high densities throughout its range and, according Tchaicka et al. (2007), total abundance could reach over 20,000,000 individuals.

In contrast, most species of Xenarthra are pres-ent at low densities in the Cerrado: E. sexcintus (0.55 ind/km²), D. novemcinctus (0.26 ind/km²), D. septem-cinctus (0.3 ind/km²), T. tricinctus (1.2 ind/km²), T. matacus (0.59 ind/km²), P. maximus (0.03 ind/km²), C. unicinctus (0.27 ind/km²), M. tridactyla (1.3 ind/km²), T. tetradactyla (0.39 ind/km²), and B. variega-tus (12.5 ind/ha; Redford & Wetzel, 1985; Hayssen, 2010, 2014; Chiarello et al., 2015). No density data are available for two species, C. didactylus and C. tatouay. The fact that xenarthrans are among the most com-mon roadkilled mammals in the Cerrado despite their low abundance underlines the gravity of road-kill to the superorder.

The large body size of Artiodactyla and Perissodactyla species probably lessens their in-cidence as roadkills because they are easily seen. Furthermore, the Brazilian Cerrado possesses only one species of Perissodactyla (Tapirus terrestris) that occurs at low densities (Gatti et al., 2011). Like

Perissodactyla, Lagomorpha presents just one spe-cies, Sylvilagus brasiliensis, which also occurs at low density.

The low occurrence of roadkilled primates al-most certainly reflects their arboreal habits (Paglia et al., 2012). Rodentia and Didelphimorphia are com-posed basically of small species that may be difficult to detect. The speed of movement during roadkill monitoring may be of great relevance here, because high speeds can underestimate taxa with small spe-cies (Dornas et al., 2012). In the studies we reviewed, 9 of 18 were performed at speeds at or above 60 km/h.

This study supports the need for a regional reas-sessment regarding the risk factors for maintaining viable populations of xenarthrans, in order to iden-tify which factors are most impacting the present state of each species. Of three species classified as threatened in the Cerrado (M. tridactyla, T. tricinctus, and P. maximus), two were recorded as roadkills. Of them, M. tridactyla had a higher incidence as road-kill than did T. tricinctus. This should not be con-sidered as a positive result for T. tricinctus because this species usually occurs at low densities in areas with high human pressures (Abba & Superina, 2010), such as roads. Therefore, every single roadkill oc-currence is a population risk factor. The situation is even more dire for M. tridactyla. According to Diniz & Brito (2015), roadkill is a serious threat to M. tri-dactyla persistence, and the removal of just a few in-dividuals may increase the possibility of population extinction.

Even if only three of the 12 Brazilian Cerrado xenarthrans are classified in threatened categories (Paglia et al., 2012), with regard to roadkill, conserva-tion strategies should take into account species that are listed as Least Concern, because over the long term the status of these species might change to a threatened category. Although xenarthrans are also threatened by other factors (e.g., habitat fragmenta-tion, uncontrolled burning, deforestation, hunting; IUCN, 2017), we believe that roadkill should be given equal weight so that measures to minimize this problem are taken and viable numbers of indi-viduals of each species are maintained.

ConclusionConstruction of wildlife overpasses and re-

duced vehicle speed in specific areas (e.g., those with high vegetation density) are measures that can re-duce the negative impacts of roadkills on xenarthran populations. In addition, educational and awareness campaigns can help, especially if they are related to the economic loss caused by roadkill. Removal of termitaria along road sides, as suggested by Freitas et al. (2014), also may minimize risk because termites are such an important part of the diet for

56 Edentata 18: 51–61 (2017)

many xenarthrans (Dalponte & Tavares-Filho, 2004; Anacleto, 2007; Cunha et al., 2015).

According to Diniz & Brito (2013), roadkill could be more dangerous than fire and inbreeding for populations of Xenarthra. Therefore, we recom-mend that roadkill be considered a “major threat” to xenarthrans in conservation status assessments.

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Received: 22 August 2017; Accepted: 3 November 2017

59P. Ribeiro et al. : The effect of roadkills on the persistence of xenarthran populations: the case of the Brazilian Cerrado

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60 Edentata 18: 51–61 (2017)

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61P. Ribeiro et al. : The effect of roadkills on the persistence of xenarthran populations: the case of the Brazilian Cerrado

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