Perspectives in Ecology and Conservation 18 (2020) 247–256

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Research Letters

Use of unfenced highway underpasses by lowland tapirs and other

medium and large mammals in central-western Brazil
Fernanda Delborgo Abra a,b,c,d,∗ , Ariel da Costa Canena c , Guilherme Siniciato Terra Garbino f ,
Emília Patrícia Medici c,d,e
a
Center for Conservation and Sustainability, Smithsonian Conservation Biology Institute, National Zoological Park, Washington, DC 20013-7012, USA
b
ViaFauna Estudos Ambientais, São Paulo, São Paulo, Brazil
c
Lowland Tapir Conservation Initiative (LTCI), Institute for Ecological Research (IPÊ), Campo Grande, Mato Grosso do Sul, Brazil
d
International Union for Conservation of Nature (IUCN), Species Survival Commission (SSC), Tapir Specialist Group (TSG), Campo Grande, Mato Grosso do Sul, Brazil
e
School of Environmental Conservation and Sustainability (ESCAS), Institute for Ecological Research (IPÊ), Nazaré Paulista, São Paulo, Brazil
f
Universidade Federal de Minas Gerais (UFMG), Instituto de Ciências Biológicas, Programa de Pós-Graduação em Zoologia, Campus Pampulha, Belo Horizonte, Minas Gerais, Brazil

h i g h l i g h t s g r a p h i c a l a b s t r a c t

• The lowland tapir was the most

recorded species using the under-
passes.
• Tapir underpass use summed more
than 180 tons of biomass that crossed
safely under the highway.
• Mammal species assemblages dif-
fered among use in cattle boxes and
drainage culverts.
• Traffic activity on the highway
peaked opposite to the activity peak
of the mammals in the crossings.
• Countries with limited finan-
cial resources should consider
retrofitting of existing highway
underpasses.

a r t i c l e i n f o a b s t r a c t

Article history: Wildlife road mortality is a worldwide problem. In tropical developing countries, it is urgent to implement
Received 25 July 2020 and test mitigation measures to reduce wildlife-vehicle collisions, especially because financial resources
Accepted 27 October 2020 are limited and alternatives should be considered such as retrofitting of existing underpasses. We assessed
Available online 11 November 2020
herein the use of 12 unfenced crossing structures, including drainage culverts and cattle boxes, by medium
and large mammals along a highway in the Brazilian Cerrado. Underpass usage was monitored for 3682
Keywords: trapping nights from September 2017 to May 2018. We recorded 20 species of medium and large wild
Lowland tapir
mammals in a total of 4212 events. The most frequent mammals were lowland tapirs (Tapirus terrestris,
Cerrado
Wildlife roadkill
n = 1154), followed by capybaras (Hydrochoerus hydrochaeris, n = 910), and crab-eating foxes (Cerdocyon
Underpass monitoring thous, n = 271). Underpass usage did not differ between drainage culverts and cattle boxes, but species
Camera-trapping composition differed among the structures, suggesting that terrestrial mammals prefer cattle boxes while
Habitat connectivity some semiaquatic species used only culverts. We identified 28 different individual tapirs using the under-
passes and we estimated over 180 tons of tapir biomass crossing under the highway. Tapir underpass

∗ Corresponding author.
E-mail address: fernanda@viafauna.com (F.D. Abra).

https://doi.org/10.1016/j.pecon.2020.10.006
2530-0644/© 2020 Associação Brasileira de Ciência Ecológica e Conservação. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://
creativecommons.org/licenses/by-nc-nd/4.0/).
F.D. Abra, A.C. Canena, G.S. Garbino et al. Perspectives in Ecology and Conservation 18 (2020) 247–256

usage did not differ between cattle boxes and culverts, but it was negatively associated with the presence
of pasture area around the structures. Our study suggests that, although underpasses show high mammal
usage suggesting a satisfactory level of connectivity, combining this method with fencing would be critical
to substantially decrease wildlife road mortality and increase human safety.

Introduction structural and functional connectivity between habitats bisected by

roads.
Many tropical areas have been extensively modified by human It is known that merely fencing the road or specific road sections
activities, including the expansion of the transportation network can be highly effective, even reducing large mammal mortality
(Gibbs et al., 2010; Foley et al., 2011; Laurance et al., 2014). At least by up to 86% (see Rytwinski et al., 2016 and references therein).
25 million kilometers of roads are planned to be built by 2050, of However, when long sections of fences are not combined with safe
which 90% are expected to occur in developing countries, including crossing opportunities, they may increase the barrier effect (Jaeger
tropical regions such as the Brazilian Amazon and Cerrado, that sus- and Fahrig, 2004; Rytwinski et al., 2016). It is also known that under
tain exceptional biodiversity and provide vital ecosystem services or overpasses without adequate fences do not reduce road mortal-
(Dulac, 2013; Laurance et al., 2014). ity effectively even if some individual animals may eventually learn
For wildlife, the effects of roads and traffic include habitat loss to use them instead of crossing the highway (Rytwinski et al., 2016;
(Forman et al., 2003; Eigenbrod et al., 2008), reduction in habitat Banhos et al., 2020).
quality in areas adjacent to the road (e.g. noise, lights, pollution, Currently, knowledge, implementation such as the studies on
visual disturbance; Forman et al., 2003; Eigenbrod et al., 2009; the efficiency of mitigation measures are geographically biased
Parris et al., 2009), barrier effect, including potential interruption toward developed countries in temperate regions. In tropical devel-
of migration and dispersion (Nellemann et al., 2001; Vistnes et al., oping countries such as in Latin America, this knowledge is still
2004; Lesbarrères and Fahrig, 2012), and direct mortality by colli- under construction, considering the intrinsic aspects of the ecology
sion with motorized vehicles (Forman and Alexander, 1998; Fahrig of tropical wildlife and their habitats (Abra, 2012; Gonzalez-Gallina
and Rytwinski, 2009). et al., 2018). Therefore, it is urgent that tropical developing coun-
The unnatural mortality of animals due to vehicle collisions is a tries implement and test the efficiency of mitigation measures to
primary, measurable, and obvious impact that can affect the demo- effectively protect their high biodiversity. Nevertheless, because
graphic structure of populations (Mumme et al., 2000; Steen and developing countries have limited financial resources and trials
Gibbs, 2004), reduce species abundance (Arévalo and Newhard, of many measures used elsewhere can be costly, mitigation alter-
2011), and create local population sinks (Nielsen et al., 2006). natives should be considered and explored, such as the use and
Most road ecology studies worldwide focus on medium and large retrofitting of existing drainage culverts, bridges, and cattle boxes
mammals, here defined as members of eight orders that have (Grilo et al., 2008).
species ≥1 kg, i.e., Artiodactyla, Carnivora, Cingulata, Didelphimor- In this study, we first assessed the use of pre-existing unfenced
phia (family Didelphidae, tribe Didelphini), Perissodactyla, Pilosa, underpasses by medium and large wild mammals in a recently
Lagomorpha, and large Rodentia (families Caviidae, Cuniculidae, paved highway (MS-040) in the Cerrado biome of central-western
Dasyproctidae, and Erethizontidae) (Van Niekerk and Eloff, 2005; Brazil. In addition, we undertook specific analyzes for lowland
Klöcker et al., 2006; Vidya and Thuppil, 2010; Huijser et al., 2013). tapirs (Tapirus terrestris), the most recorded species of this study.
Besides their important ecological roles (Cuarón, 2000; O’Farrill Tapirs have a double appeal in the context of reduction of mammal-
et al., 2013), medium and large mammals can also cause serious vehicle collision. First, they provide important ecosystem services
vehicle collisions, risking human safety and generating economic through seed dispersal and maintenance of biodiversity and ecosys-
losses for drivers, passengers, and road managers (Conover et al., tem services (Paolucci et al., 2019). Second, in the context of road
1995; Bruinderink and Hazebroek, 1996; Huijser et al., 2008; Abra ecology, tapirs can weigh up to 300 kg, with females being larger
et al., 2019). than males (average, male = 180 kg, female = 200 kg), and have the
Collisions between mammals and vehicles have increased over potential to cause severe road accidents (Medici, 2011; Medici et al.,
the last decades. In North America, for example, wildlife-vehicle 2016; Medici and Abra, 2019). A recent accident involving a tapir
collisions increased 4-fold in the last 50 years. In the Brazilian in the studied highway, resulted in three human deaths and one
state of São Paulo, animal-vehicle collisions jumped from about severe injury due to a collision between a van and a truck (July
138,000 in 2003 to 150,000 in 2012 and wild mammal road mor- 8, 2020; G1, 2020). Considering the landscape configuration, we
tality increased 65% from 2009 to 2014 (Abra, 2019; Abra et al., asked if differences in passage use by tapirs were related to measur-
2019; Hill et al., 2020). In this scenario, different efforts have been able environmental variables. Ultimately, the study design allowed
carried out to justify, plan, design, and fund effective mitigation us to address current and basic questions related to wildlife using
measures. crossing structures in Brazil.
Worldwide, there are more than 40 different types of mitigation
measures available, but the most common and robust measures Methods
are the combination of fences and safe crossing opportunities,
such as underpasses and overpasses, which are widely used in Study area
North America and Europe (Gloyne and Clevenger, 2001; Cain et al.,
2003; Clevenger and Waltho, 2005; Mata et al., 2005; Huijser et al., The study was carried out along a ca. 50 km stretch of the MS-
2016; Gonzalez-Gallina et al., 2018). When implemented and main- 040 highway in Mato Grosso do Sul State in central-western Brazil,
tained correctly, these fenced passages were found to reduce up between September 2017 and May 2018 (Fig. 1). This State encom-
to 97% of the large mammal–vehicle collisions, especially North- passes three different biomes, the Atlantic Forest, Cerrado and
American and European ungulates (Sawyer et al., 2012; Gagnon Pantanal (wetland), with 166 mammal species recorded (Tomas
et al., 2015; Huijser et al., 2016). Wildlife passage systems have et al., 2017). We selected this specific site based on preliminary
two distinct roles: first, the fences block the animals’ access to reports categorizing this stretch of highway as a hotspot for lowland
the road and thus, guide them to a safe crossing structure; sec- tapir roadkill (Medici et al., 2016). The MS-040 highway is 220 km
ond, the crossing structure has the potential to reestablish the long and connects the capital city of the state, Campo Grande, to

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Fig. 1. Underpasses along Highway MS-040 in Mato Grosso do Sul State, Brazil.

a smaller county, Santa Rita do Pardo. The highway has two-lanes Table 1
Characteristics of monitored underpasses along Highway MS-040 in Mato Grosso
with no shoulders. The average speed limit is 80 km/h. Along its
do Sul State, Brazil.
entire length, there are 52 underpasses of which 12 were monitored
during this study including: seven cattle boxes, four culverts, and ID Structure WP Width × height (m)
one bridge. All 12 underpasses are inside the main roadkill hotspot 1 CB No 2 × 2.5
for lowland tapirs. The region crossed by the highway is domi- 2 DC Yes 2.5 × 2.5
nated by cattle pastures and agriculture, as well as small patches of 3 CB No 3×3
4 Bridge Yes 30 × 6
Cerrado vegetation and riparian forests. The climate is seasonally
5 CB No 2×2
characterized by a rainy season from October to March, with an 6 DC Yes 2×2
average annual rainfall of 1,250 mm (range 1,000–1,500 mm) and 7 CB No 2×2
a drier period from April to September (Koppen’s As or Aw). 8 DC Yes 2×2
9 CB No 2×2
Some studies on roadkill of medium- and large-sized mammals
10 CB No 2×2
have been carried out on this highway, mainly by Brazilian con- 11 DC Yes 2.5 × 2.5
servation projects Lowland Tapir Conservation Initiative (LTCI) – 12 CB No 2×2
Institute for Ecological Research (IPÊ) and “Anteaters & Highways CB = cattle box, DC = drainage culvert, WP = water presence.
Project” (Medici et al., 2016; Ascensão et al., 2019; Medici and Abra,
2019).
The upgrade of the MS-040 highway was completed in Novem- totaling 24 cameras. The cameras were placed at an approximate
ber 2015, turning a dirt road into a two-lane paved highway. height of 50 cm above the ground and installed outside of the
New cattle underpasses were built to reconnect cattle herds from underpasses but directed towards the entrances of the structures,
ranches bisected by the highway. In the environmental licensing to allow the recording of the animals’ acceptance and rejection
process required for this upgrade, mitigation measures were rec- crossings rates (Fig. 2d). The cameras were programmed to capture
ommended to reduce wildlife road mortality and increase human a sequence of nine photos and/or videos of 30 s from the detection
safety but have yet to be implemented. of the animal by the sensor, with an interval of five seconds between
The transportation agency responsible for maintaining the high- sequences, and were kept in full-time operation for 263 days from
way (AGESUL – Agência Estadual de Gestão de Empreendimentos) did September 2017 to May 2018. Memory cards and rechargeable bat-
not implement the mitigation measures and the Mato Grosso do Sul teries were replaced every 15 days.
State environmental agency (IMASUL – Instituto de Meio Ambiente
de Mato Grosso do Sul) did not investigate the non-compliance with Tapir data collection
such measures. Both agencies are currently the target of a public
civil lawsuit filed by the Brazilian Attorney General’s Office of Mato Camera-trap records of tapirs were carefully screened by two
Grosso do Sul State in 10 million Brazilian Reais (∼US$ 2.63 million) tapir specialists and authors of this study (EPM and ACC) for sexing,
(Medici and Abra, 2019). age class estimation and social organization of the animals (repro-
ductive pairs, females with young). Whenever possible, individual
Underpass wildlife monitoring tapirs were identified through unique morphological patterns in
each individual (e.g. natural marks, scars and fissures on the ear,
A total of 12 underpasses (seven cattle boxes, four drainage cul- shape of the tail and pelvic girdle, shape of the head, extension, and
verts and one bridge) were monitored with camera-traps (Stealth height of the mane). During the monitoring of the underpasses, we
Cam STC-G34, motion sensor) (Fig. 2, Table 1). We used two cam- also recorded the number of opportunistic sightings of live tapirs
eras per passage, one in each entrance on both sides of the highway, and road killed tapir carcasses along highway MS-040.

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Fig. 2. Types of underpasses monitored along Highway MS-040 in Mato Grosso do Sul State, Brazil: (a) drainage culvert, (b) cattle box, (c) bridge and (d) view of drainage
culvert, red circle shows the installation of the camera-trap outside of the structure.

Traffic volume counts boxes were compared in relation to the tapir usage index using
Wilcoxon rank sum tests (P < 0.05).
As there are no official traffic volume counts for highway We calculated the estimated tapir mass that used the under-
MS-040, we carried out vehicle counting following the Federal passes, including complete and unknown crossings, during the
Transportation Agency methodology (DNIT, 2020). We undertook study period, using the mean body mass for adults (male = 180 kg,
15 sessions of data collection at three different points along the female = 200 kg), subadults (100–180 kg), and juveniles (70 kg)
highway (km 28, km 100 and km 150), including five 24-hour peri- based on the dataset of the Lowland Tapir Conservation Initiative.
ods in each point. Data were collected on weekdays, weekends, The relationship between complete and unknown crossings, and
and holidays. The averaged traffic volume data was compared to the detection by camera traps were also used to determine the
the usage time of wildlife in the underpasses. presence and diversity of user species, as well as the anthropic
influence.
To verify the influence of landscape attributes on the usage
Data analyses index of tapirs, we used every structure (n = 11) except for the
bridge, which we excluded because it had significantly differ-
We quantified the use of crossing structures by mammals using ent dimensions. We measured the following landscape attributes
descriptive analyses. The usage index was calculated by sum- (in hectares) within a 1 km radius of each underpass: pasture
ming the number of complete and unknown crossings by a given area, native forest area, and grassland area (MapBiomas Project
mammal species divided by the number of days the passage was Collection 4.1; 30 m resolution; using ArcGIS ESRI, 2015). To verify
monitored. We considered independent events to be consecutive the influence of domestic livestock on the passage of tapirs, we also
photographs or videos of the same species separated by at least 1 h quantified the usage index of cattle.
(Tobler et al., 2008). To analyze the usage index as a function of the covariates, we
We classified the events in the underpasses in three categories: conducted four pairwise linear regression analyses, as our response
(i) complete crossing, when it was possible to confirm the entrance variable (usage index) had a Gaussian distribution: 1) tapir usage
and exit of the same individual by the two camera traps; (ii) index on forest cover (continuous), (2) tapir usage index on pas-
unknown crossing, when animals were recorded by at least one ture cover (continuous), (3) tapir usage index on grassland cover
of the cameras with a clear behavior of entering and leaving the (continuous), (4) tapir usage index on cattle usage index (rate).
underpass; (iii) no-crossing, when the presence of individuals was
recorded but with a clear behavior that the animal did not cross the
underpass. Results
Alpha diversity indices were calculated using the independent
events. We calculated the species richness (Sobs) 0 D, Shannon’s Underpass wildlife monitoring
exponential index (eH ) 1 D, and the Inverse Simpson’s index (1/D)
2 D for all camera trap stations and compared the indexes between From September 2017 to May 2018, we carried out 3,682 trap-
the cattle boxes and culverts. ping nights and recorded 20 species of medium- and large-sized
For tapir-specific analyzes, including complete crossings and wild mammals visiting the underpasses (Table 2, Appendix 1).
unknown crossings, the 12 sampled passages were divided in three Considering only independent events, a total of 4,212 individ-
categories: culverts, cattle boxes, and bridge. Culverts and cattle uals were recorded, for a rate of 114.39 events/100 trap nights.

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Table 2
Mammal use of underpasses along Highway MS-040 in Mato Grosso do Sul State, Brazil. The crossing rate was calculated for both complete and unknown crossings.

Mammal species Crossings

Threat category Usage Type of NC C (n, %) U C (n, %) C C (n, %) N◦ Ind. (n, %)

(trend) index passages
used

Lowland tapir (Tapirus VU (H) 0.27 CB, DC, B 146; 5.67% 510; 19.80% 498; 10.33% 1,154; 44.80%
terrestris)
Capybara (Hydrochoerus LC ( ) 0.20 DC, B 155; 6.02% 538; 20.89% 217; 8.42% 910; 35.33%
hydrochaeris)
Crab-eating fox (Cerdocyon LC ( ) 0.06 CB 34; 1.32% 158; 6.13% 79; 3.07% 271; 10.52%
thous)
Giant anteater VU (H) 0.02 CB, B 6; 0.23% 57; 2.21% 35; 1.36% 98; 3.80%
(Myrmecophaga tridactyla)
Yellow armadillo LC ( ) 0.0081 CB 6; 0.23% 27; 1.05% 3; 0.12% 36; 1.40%
(Euphractus sexcinctus)
Azara’s agouti (Dasyprocta DD (H) 0.0065 CB, 4; 0.16% 24; 0.93% 0; 0% 28; 1.09%
azarae)
Crab-eating racoon LC (H) 0.0057 CB, DC, B 4; 0.16% 9; 0.35% 12; 0.47% 25; 0.97%
(Procyon cancrivorus)
Ocelot (Leopardus pardalis) LC (H) 0.0030 CB 1; 0.04% 9; 0.35% 2; 0.08% 12; 0.47%
Maned wolf (Chrysocyon NT (?) 0.0011 CB 2; 0.08% 2; 0.08% 2; 0.08% 6; 0.23%
brachyurus)
Water opossum LC (H) 0.0011 DC 1; 0.04% 4; 0.16% 0; 0% 5; 0.19%
(Chironectes minimus)
Nine-banded armadillo LC ( ) 0.0014 CB 0; 0% 5; 0.19% 0; 0% 5; 0.19%
(Dasypus novemcinctus)
Southern naked-tail LC (?) 0.0011 CB 0; 0% 4; 0.16% 0; 0% 4; 0.16%
armadillo (Cabassous
unicinctus)
Pantanal cat (Leopardus NA(NE) 0.0011 CB 0; 0% 4; 0.16% 0; 0% 4; 0.16%
braccatus)
Giant armadillo (Priodontes VU (H) 0.008 CB, B 1; 0.04% 2; 0.08% 1; 0.04% 4; 0.16%
maximus)
Tayra (Eira barbara) LC (H) 0.003 CB 2; 0.08% 0; 0% 1 3; 0.12%
Neotropical otter (Lontra NT (H) 0.008 DC 0; 0% 3; 0.12% 0; 0% 3; 0.12%
longicaudis)
Gray brocket deer (Mazama LC (H) 0 - 3; 0.12% 0; 0% 0; 0% 3; 0.12%
gouazoubira)
Southern tamandua LC (?) 0.008 CB 0; 0% 3; 0.12% 0; 0% 3; 0.12%
(Tamandua tetradactyla)
Southern American Coati LC (H) 0.003 CB 0; 0% 1; 0.04% 0; 0% 1; 0.04%
(Nasua nasua)
Collared peccary (Pecari LC ( ) 0 - 1; 0.04% 0; 0% 0; 0% 1; 0.04%
tajacu)
Total 366; 1,360; 52.80% 850; 33% 2,576; 100%
14.21%

NC C = not completed crossing, U C = unknown crossing, C C = completed crossing, N◦ Ind. = number of individuals, VU = vulnerable, LC = least concern, DD = data deficient,
NT = near threatened, NA = not assessed. Population trend: H = decreasing, = stable and ? = unknown, NE = not evaluated. Type of passages used: CB = cattle box, DC = drainage
culvert, B = bridge.

Records included wild mammal species (n = 2,666; 63.3%), domes-

tic species (n = 883; 20.97%), and humans (n = 663; 15.7%). The most
frequent wild mammal was the lowland tapir (n = 1,154; 44.8%),
followed by the capybara (n = 910; 35.33%), and the crab-eating
fox (n = 271; 10.52%) (Fig. 3). Two species, the coati (Nasua nasua)
and collared peccary (Pecari tajacu), were recorded only once dur-
ing the study period (Table 2). Three of the recorded species,
i.e., lowland tapir, giant armadillo (Priodontes maximus), and giant
anteater (Myrmecophaga tridactyla), are classified as “Vulnerable”
to extinction in both the Brazilian Red List and the IUCN Red List
of Threatened Species (Medici et al., 2018; IUCN, 2019). Our survey
recorded 33% of the threatened mammals that potentially occur in
the study area (Tomas et al., 2017).
Mean underpass usage index for all wild mammal species Fig. 3. Relative frequency of medium- and large-sized mammals sampled at the 12
lumped together was 0.47, varying from 0.26 for tapirs to zero monitored underpasses along Highway MS-040 in Mato Grosso do Sul State, Brazil.
for gray brocket deer (Mazama gouazoubira) and collared peccary, Only species with ≥10 independent records are shown.
which were recorded by the cameras but did not enter the culvert
(Table 2). The Wilcoxon rank sum test did not recover a statis-
tically significant difference (W = 7, P = 0.2, r = 0.39) between the boxes, considering both species richness (W = 27, P = 0.017, r = 0.75)
number of individuals using culverts and cattle boxes (Fig. 4). How- and proportional abundances, as inferred by Shannon’s exponen-
ever, overall species diversity was significantly higher at cattle tial (W = 28, P = 0.006, r = 0.79) and Inverse Simpson’ index (W = 27,
P = 0.01, r = 0.74; Fig. 5).

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Fig. 6. Frequency of records for vehicle counting and complete and incomplete
crossing of wild mammals and tapirs based on traffic counts made between Septem-
ber and December 2017 along Highway MS-040 in Mato Grosso do Sul State, Brazil.

Fig. 4. Usage index of all 18 species of wild mammals and of only tapirs at both
crossing structures analyzed along Highway MS-040 in Mato Grosso do Sul State,
Brazil. Bars indicate mean values for each structure and lines are the mean + standard days) and the calf stays with its mother for 12–18 months (Medici,
deviations. NS = non-significant (P > 0.05).
2011). Both male and female tapirs reach sexual maturity at four
years of age. The tapir life span in the wild is estimated to be 20–25
years (Medici and Desbiez, 2012). During this study, five repro-
ductive pairs and four females with calves were detected. Tapirs
are wide-ranging species, and this methodology has allowed us to
observe that at least seven individuals used more than one under-
pass, in which cases the structures were close or adjacent to each
other (ca. 2 km). Moreover, the bridge was used by at least eight
different tapir individuals followed by underpasses ID-7 and ID-8
which were used by seven different tapir individuals each.
In 11 of the 12 structures, tapirs crossed to the opposite side
of the highway. Although there were no differences between the
usage of cattle boxes and culverts (W = 14, P > 0.1, r = 0.45; Fig. 4),
some passages were more intensely used than others (Fig. 7).
The 2,210 tapir crossing events represent a total of 186,010 kg of
tapirs using the structures (x¯ = 15,500 kg, ±13,129), ranging from
36,480 kg in a single underpass to zero. Tapir usage was most
intense between km 120 and km 140 of the MS-040 highway.
Fig. 5. Medium- and large-sized mammal diversity profile for two types of cross-
Univariate regressions suggest that the usage index of the pas-
ing structures analyzed along Highway MS-040 in Mato Grosso do Sul State,
Brazil. 0 D = species richness, 1 D = Shannon’s exponential index, 2 D = Inverse Simp- sages by tapirs was negatively correlated with the area of pasture
son. * = significant for P < 0.05; ** = significant for P < 0.01. around the underpass which represents 79% of the land use (Fig. 8).
The index of underpass usage by tapirs also had a weak negative
correlation with the cattle usage index, and a weak positive asso-
Despite the differences in diversity of species between cattle
ciation with the area of forest and native grasslands around the
boxes and culverts, some species were recorded only in culverts
structures which correspond to 19% of land use (Fig. 8).
and vice-versa. The semi-aquatic river otter (Lontra longicaudis) and
During the study period, we recorded seven direct tapir sight-
water opossum (Chironectes minimus), for example, were recorded
ings along the monitored highway section. In most cases, the
only in culverts, while terrestrial wild canids and felids, were
animals crossed the highway using the pavement (Fig. 9a). In addi-
recorded only in cattle boxes (Table 2).
tion, we recorded 21 road-killed tapirs in the same period along
highway MS-040, of which nine were found within the 50 km of
Traffic volume × mammal crossing time
the monitored highway section (Fig. 9b).

Vehicle traffic was high between 6 am and 6 pm with peaks at

8 am and 5 pm, being the activity during this period amounting Discussion
to 82.62% of the total traffic volume in MS-040 (Fig. 6). The activ-
ity period of medium- and large-sized mammals, including tapirs, This study shows that unfenced underpasses are suitable for
peaked in opposite times of traffic volume. For mammals in gen- crossings by large and medium-sized mammals, especially tapirs,
eral, the peak was at 4 am and 6 pm, while for tapirs it was between from the point of view of the maintenance of connectivity. Our
3–5 am and 7–8 pm. results suggest the possibility of retrofitting the existing under-
passes, which were originally built for other purposes than wildlife
Tapir crossing analyses crossings, i.e., for water drainage and for cattle passage (Grilo et al.,
2008; Huijser et al., 2013). The main advantage of using these pas-
Through photo-identification, it was possible to recognize 28 sages is that they are cost-effective for highway managers, as the
individual tapirs, of which 25 were adults, two juveniles and one structures have already been built. Drainage culverts are neces-
calf. Among these, 12 females and 16 males were identified. Tapirs sary to route water under the road, cattle boxes are required by
are primarily solitary, although it is common to sight reproductive local landowners to provide connectivity for domestic animals and
pairs and females with offspring. Tapirs usually produce a single off- people. Primarily for developing countries, the retrofitting of exist-
spring after a lengthy gestation period of 13–14 months (390–410 ing underpass structures can be valuable in encouraging highway

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Fig. 7. Heatmap of the 12 monitored underpasses along Highway MS-040 in Mato Grosso do Sul State, Brazil, showing the amount of tapir mass (kilograms) that used the
structures.

Fig. 8. Univariate regressions of tapir usage index (response variable), and four independent variables.

managers to implement measures aimed at reducing wildlife road ciently reduce road mortality, it is highly recommended to install
mortality. fences in combination with underpasses, as studies suggest that
The lowland tapir was the most recorded species using the this measure can reduce up to 86% of mammal-vehicle collisions
underpasses in our study. All tapir individuals registered using the as demonstrated in Highway 93 in Montana, United States (Huijser
underpasses summed more than 180 tons of biomass that crossed et al., 2016) and other regions in North America and Europe (see
safely under the highway. This means that passages are already Rytwinski et al., 2016 and references therein).
being used and have certainly reduced the number of tapirs on the Underpasses close to natural Cerrado fragments and bodies of
lanes and increased traffic safety. However, because the highway water were more relevant for tapir crossings. These areas reflect a
is not fenced, it is not possible to verify if tapirs were using the more appropriate tapir habitat (Medici, 2011), as the study site is
underpasses more than crossing on the highway. In order to effi- largely dominated by agriculture and pasture. In Mato Grosso do

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Fig. 9. (a) Lowland tapir crossing Highway MS-040, and (b) Tapir roadkill on the same highway. Source: Laurie Hedges, INCAB-IPÊ.

Sul State, cattle management demands human presence and both to implement fences becomes more urgent when medium and large
studied variables (pasture area and cattle usage index) were nega- mammals routinely use areas adjacent to highways, as is the case in
tively associated to tapir crossings, corroborating previous studies our study area. To increase the diversity of medium and large mam-
(Land and Lotz, 1996; Clevenger and Waltho, 2000; Ng et al., 2004). mals using the underpasses, we recommend implementing distinct
Even though our findings did not detect differences in the num- types of underpasses along the roads, as some semiaquatic species
ber of individuals using drainage culverts or cattle boxes, species depend on water bodies to disperse and some terrestrial mammals
composition differed among the structures, suggesting that, in prefer dry structures. Evidently, it is highly recommended that such
general, terrestrial mammals prefer cattle boxes while some semi- measures are monitored to ensure accurate information about their
aquatic species such as capybara, water opossum and river otter efficiency in reducing road mortality and increasing connectivity
rarely venture in dry passages. Both types of underpasses have for these species.
the same approximate dimensions (∼2 x 2 m) and based in our
results their size seems suitable for species registered more fre- Acknowledgements
quently in the structures as lowland tapir, capybara, crab-eating
fox, giant anteater, and yellow armadillo, among others. Some The evaluation and mitigation of wildlife roadkill has been an
species, namely collared peccary, gray brocket, coati, neotropi- important component of the long- term activities of the Lowland
cal otter and southern tamandua, had only a few records but Tapir Conservation Initiative (LTCI) - Instituto de Pesquisas Ecológ-
are not considered rare in the study area, and some of them are icas (IPÊ) in Brazil. The LTCI has the institutional support from the
even recorded in roadkill reports (Ascensão et al., 2017, 2019). IUCN SSC Tapir Specialist Group, Association of Zoos and Aquar-
Moreover, some of these least common species in our study area iums Tapir Taxon Advisory Group, and European Association of
were frequently reported in other underpasses studies in central- Zoos and Aquariums Tapir Taxon Advisory Group. Over the years,
western São Paulo state, Brazil (Abra, 2012). The coati, for example, the LTCI has been funded by several national and international
accounted for 8.8% of all mammal crossings in the São Paulo study agencies including over 50 zoological institutions, 20 NGOs and
site (Abra unpublished data). Because we had data for one bridge foundations, 15 private businesses as well as private individuals.
only, it was not statistically possible to include it in the analysis, The main supporters of the LTCI Cerrado Program are Fondation
but the number of individuals and species richness recorded sug- Segré, Houston Zoo, and Whitley Fund for Nature. The Instituto
gest that the bridge is a very important structure for wildlife use. As Chico Mendes de Conservação da Biodiversidade (ICMBIO- SISBIO)
bridges cross over large water bodies, they are usually associated provides the required research permits. The authors would like to
with riparian vegetation, a type of habitat widely used as ecological thank André Regolin and Gabriela Rezende for their support with
corridors in fragmented landscapes for wildlife dispersal, foraging statistical analysis.
and shelter (Lees and Peres, 2008). Riparian forests are one of the
most important habitats for tapirs (Medici, 2010). Appendix 1.
The peak of traffic activity on the MS-040 highway was between
6 am and 6 pm, quite the opposite of the activity peak of the mam- Mammal species recorded in the underpasses along High-
mals (including tapirs) recorded in the crossings. Specifically, for way MS-040 in Mato Grosso do Sul State, Brazil: a. Azara’s
tapirs, the time of use in the underpasses matches the activity agouti (Dasyprocta azarae), b. Southern tamandua (Tamandua
patterns previously recorded for the species in Brazil, Bolivia, and tetradactyla), c. South American coati (Nasua nasua), d. Human use,
Peru (Noss et al., 2003; Tobler, 2008; Medici, 2010; Medici, 2011). e. Cattle (Bos indicus), f. Horse (Equus caballus), g. Domestic dog
In general, medium and large mammal species show nocturnal (Canis lupus familiaris), h. Yellow armadillo (Euphractus sexcinctus),
and crepuscular activity but it is tempting to suggest that some i. Gray brocket deer (Mazama gouaboubira), j. Southern naked-
species may be avoiding the peak traffic activity along the high- tail armadillo (Cabassous unicinctus), k. Ocelot (Leopardus pardalis),
way due to noise, motion, and visual disturbance (Gaynor et al., l. Capybara (Hydrochoerus hydrochaeris), m. Giant armadillo (Pri-
2018). odontes maximus), n. Giant anteater (Myrmecophada tridactyla), o.
Although the underpasses seem to be suitable to maintain wild Crab-eating racoon (Procyon cancrivorus), p. Neotropical otter (Lon-
mammal permeability and safeguard a satisfactory habitat con- tra longicaudis), q. Maned wolf (Chrysocyon brachyurus), r. Pampas
nectivity, we suggest that the use of fences would be critical to cat (Leopardus braccatus), s. Collared peccary (Pecari tajacu), t. Crab-
further decrease mortality of both humans and wildlife. The need eating fox (Cerdocyon thous).

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