Effect of free-ranging cattle on mammalian diversity: an Austral Yungas case study
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Effect of free-ranging cattle on mammalian diversity:
an Austral Yungas case study
GRIET AN ERICA CUYCKENS, NOELIA VIVIANA GONZALEZ BAFFA TRASCI
P A B L O G A S T Ó N P E R O V I C and L U C I O R I C A R D O M A L I Z I A
Abstract Extensive cattle ranging is an important economic Introduction
activity in mountains, with diverse effects on native mam-
mal communities. The effects of cattle Bos taurus can be
negative, positive or neutral, mostly depending on the stock- F ree-ranging cattle affect native fauna, species interac-
tions and ecological communities across geographical re-
gions in a variety of ways (Elliott & Barrett, ; Moser &
ing rate. We examined the effect of cattle on the diversity
and abundance of native mammalian species in the Witmer, ; Hettinger, ; Pia et al., ; Shepherd &
Austral Yungas region of Argentina, considering environ- Ditgen, ; Chaikina & Ruckstuhl, ). In forest
mental variables, land protection status, and human influ- ecosystems in Australia, the presence of free-ranging cattle
ence. Using , trap-nights from camera-trap negatively affects vegetation regeneration by compacting
stations over years (–), we calculated a relative the soil through trampling and diminishing the abundance
abundance index using camera events and used generalized of seedlings by grazing (Eldridge et al., ). In South
linear models to estimate the effect of cattle on small mam- American forests, the effect of cattle Bos taurus is hetero-
mals, large herbivores, species of conservation concern and geneous and studies have been restricted to a few forest eco-
felids. Cattle had different effects on each group of native systems and ecological variables (Mazzini et al., ).
mammals. We observed a lower abundance of large native The intensive use of the forest understorey by cattle can
herbivores and the absence of small mammals in areas cause a reduction in plant biomass, potentially reducing the
with high cattle abundance. The tapir Tapirus terrestris, jag- complexity of the understorey (Loeser et al., ) and in-
uar Panthera onca and white-lipped peccary Tayassu pecari creasing the density of shrubs resistant to browsing
are rare in the Yungas and therefore potentially vulnerable (Vandenberghe et al., ), thus changing forest structure
to extinction there. Conservation of small felids and low cat- and composition. These changes in vegetation could have
tle abundance could be compatible, but felids are threatened both direct and indirect effects on native mammal biodiver-
by other anthropogenic influences. Native mammalian di- sity. By affecting the understorey of forests and reducing ref-
versity and richness were related to land protection status. uge and food availability, cattle have the potential to affect
The entire ecoregion is potentially suitable for cattle, sug- small forest mammals negatively (Tabeni et al., ). Cattle
gesting the potential for further threats, and that cattle may also affect large native herbivores by reducing food
should be excluded from strictly protected areas. To ensure diversity and competing for pastures (Madhusudan,
extensive cattle ranging is compatible with wildlife conser- ). By altering small mammal abundance (i.e. prey for
vation in areas where exclusion is not possible, we recom- carnivores), cattle also cause cascading effects on higher
mend improved management of cattle and moderate trophic levels (Pia et al., ).
stocking rates. The influence of cattle is not straightforward (Hettinger,
) and is mainly determined by the stocking rate
Keywords Bos taurus, cattle, empty forest, human foot- (Schieltz & Rubenstein, ). Mammalian species exhibit
print, livestock, national parks, niche-based distribution different responses linked to their specific life traits
modelling, threatened species (Suraci et al., ). Forest specialist mammal species decline
Supplementary material for this article is available at rapidly when forest cover decreases and are unlikely to be
doi.org/./S found in secondary forests, whereas non-specialists survive
in human-modified habitats (Newbold et al., ), and
some species such as the white-eared opossum Didelphis al-
biventris and Molina’s hog-nosed skunk Conepatus chinga
GRIET AN ERICA CUYCKENS (Corresponding author, orcid.org/0000-0002-9019- could benefit from cattle-modified habitat (Di Bitetti et al.,
8916, grietcuyckens@yahoo.com), NOELIA VIVIANA GONZALEZ BAFFA TRASCI
( orcid.org/0000-0001-5666-8614) and LUCIO RICARDO MALIZIA Instituto de ).
Ecorregiones Andinas–Universidad Nacional de Jujuy, Consejo Nacional de To ensure the protection of biodiversity, a total exclusion
Investigaciones Científicas y Tecnológicas and Centro de Estudios
Territoriales Ambientales y Sociales, Alberdi 47, 4600 San Salvador de Jujuy,
of cattle and strict controls against hunting are imposed
Argentina by national parks in Argentina (IUCN category II pro-
PABLO GASTÓN PEROVIC Administración de Parques Nacionales, Salta, Argentina tected areas). Other categories (VI) allow traditional cattle
Received December . Revision requested July .
raising. In regions where cattle are managed extensively
Accepted October . and with little veterinary control, the management of a
This is an Open Access article, distributed under the terms of the Creative Commons-Attribution-ShareAlike licence (https://creativecommons.org/licenses/by-sa/4.0/), which permits re-use,
distribution, reproduction, transformation, and adaptation in any medium and for any purpose, provided the original work is properly cited and any transformation/adaptation is distributed
under the same Creative Commons licence.
Oryx, 2022, 56(6), 877–887 © The Author(s), 2022. Published by Cambridge University Press on behalf of Fauna & Flora International doi:10.1017/S0030605321001538
https://doi.org/10.1017/S0030605321001538 Published online by Cambridge University Press
878 G. A. E. Cuyckens et al.
site plays a fundamental role in the local stocking rate, and Species groups
therefore in fauna conservation (Schieltz & Rubenstein,
). Of the recorded species, we selected four groups that can
Since the s, the range of domestic cattle in Argentina potentially be influenced by cattle. By reducing refuge and
has expanded into areas marginal for agriculture, mostly food availability for small mammals (Tabeni et al., ),
forested areas (Guevara et al., ) such as the Austral we expected a negative influence of cattle on the presence
Yungas in the north-west. In the Argentine Yungas, cattle and relative abundance of small mammal species. In
raising entails releasing cattle into the forests, without nu- this group we included unidentified small mammals
tritional supplements and with little to no management (i.e. # kg), the agouti Dasyprocta sp. and the tapeti
(Quiroga et al., ). This extensive ranging of livestock, Sylvilagus brasiliensis. Cattle may also affect large native
combined with selective logging and firewood extraction, herbivores by reducing food diversity and competing for
has adverse effects on the structure of native forests pastures (Madhusudan, ). In the large herbivore species
(Campanello et al., ; Blundo et al., ). However, group we included the red brocket deer Mazama americana
the effect of cattle has not been considered as an explanatory and gray brocket deer Mazama gouazoubira. We expected a
variable when examining patterns of mammalian diversity, lower relative abundance of both species with higher cattle
nor is it known how cattle affect fauna in one of the most abundance, and absence of the species at a certain, un-
biodiverse ecosystems in Argentina. known, threshold of cattle abundance. We predict similar
We aimed to assess the effect of cattle on the native mam- effects on these two species, and therefore we pooled data
malian community of the Austral Yungas and any potential for a more robust statistical analysis. For species of conser-
interaction with altitude, latitude and land protection status. vation concern we included threatened species based on
We considered four species groups: small mammals, large national and/or international standards (Ministerio de
herbivores, species of conservation concern and the felid Ambiente y Desarrollo Sostenible & Sociedad Argentina
community. We also examined the potential of cattle to in- para el Estudio de los Mamíferos, ; IUCN, ): the
habit the Yungas ecoregion on a regional scale. We expected lowland tapir Tapirus terrestris, white-lipped peccary Tayassu
() lower mammalian richness and diversity at higher alti- pecari and jaguar Panthera onca. Based on the potential
tudes, increasing latitude and in areas of lower protection influence of cattle on the relative abundance of small mam-
status, () lower abundance or absence of the four species mals and cascading effects on higher trophic levels (Pia
groups in areas with greater cattle abundance and anthropo- et al., ), we expect a negative influence of cattle on the
genic influence, and () that cattle could potentially inhabit presence and relative abundance of small and medium-
the entire Yungas ecoregion. sized felids. This group comprised the medium-sized ocelot
Leopardus pardalis, and five small felids: jaguarundi
Herpailurus yagouaroundi, Pampas cat Leopardus colocolo,
Geoffroy’s cat Leopardus geoffroyi, oncilla Leopardus
Study area
tigrinus and margay Leopardus wiedii (Table ).
The study area is the Austral Yungas of Argentina (sensu
Brown & Pacheco, ) on the eastern slope of the Andes. Camera-trap survey
This ecoregion is characterized by subtropical cloudy
montane forests and has an altitudinal gradient of vege- We placed camera stations: in national parks, in
tation physiognomy and species composition (Brown et al., provincial reserves, in private protected areas, in
). The Yungas is considered a vulnerable ecosystem private lands without protection, in state properties
(Olson & Dinerstein, ) of high conservation value without management, and nine in Indigenous territories.
(Malizia et al., ) because of the high faunal diversity The trapping period was January – September
(Narosky & Yzurieta, ; Ojeda, ). Cattle were intro- (, effective trap-nights). We recorded geographical
duced into the region c. years ago (Brown & Grau, ), coordinates and altitude at each point using a GPS.
but their distribution is limited by the terrain and therefore Camera-trap stations consisted of one camera, generally
cattle density is highly variable. located along a trail, road or river bank, to optimize the
capture of larger mammals, which prefer to walk along lin-
ear features (Harmsen et al., ). In some cases, to ensure
Methods cameras were not interfered with or stolen, we placed
them in the forest interior. The mean distance between
We surveyed using camera traps across latitudinal and nearest neighbouring cameras was . ± SD . km. Cam-
altitudinal gradients in areas with forest cover (Fig. ). eras were programmed to obtain a set of three photographs,
To measure the success of our method, we developed a po- with a -minute delay between successive sets, and were
tential species list for the Yungas forests (Table ). active continuously.
Oryx, 2022, 56(6), 877–887 © The Author(s), 2022. Published by Cambridge University Press on behalf of Fauna & Flora International doi:10.1017/S0030605321001538
https://doi.org/10.1017/S0030605321001538 Published online by Cambridge University PressEffect of free-ranging cattle on mammalian diversity 879
FIG. 1 Study area and location
of camera traps in the Austral
Yungas of Argentina. Size of
circles indicates the number of
native mammalian species
recorded per camera trap.
Environmental variables brooks, rills and runnels). All variables were projected
to the WGS datum and were at a spatial resolution of
We used bioclimatic variables (Karger et al., ). From arc-seconds or resampled at this pixel size, equivalent
altitude, we derived slope and roughness, using QGIS .. to c. km.
(QGIS, ), which we also used for all other geographical
analyses. We obtained the human influence index from
WCS & CIESIN (); this index incorporates human Mammalian diversity
population pressure, human land use, infrastructure and
human access. Values range from (no influence) to We identified all large and medium-sized animals recorded
(maximum influence). We obtained the coupled evapo- by the camera traps to species level, noting whether they
transpiration and gross primary production (hereafter re- were native or exotic, and calculated diversity indices for
ferred to as primary production) from the National the native species. Records were considered independent
Tibetan Plateau Data Center (Zhang et al., , ; when they were at least h apart. From the number of events
Gan et al., ), and we generated Euclidean distances and effort (i.e. the number of effective camera-trap nights
from cameras to the nearest water line (rivers, streams, of each camera), we calculated the relative abundance
Oryx, 2022, 56(6), 877–887 © The Author(s), 2022. Published by Cambridge University Press on behalf of Fauna & Flora International doi:10.1017/S0030605321001538
https://doi.org/10.1017/S0030605321001538 Published online by Cambridge University Press880 G. A. E. Cuyckens et al.
TABLE 1 Species of large and medium-sized native and exotic mammals that could potentially occur in the Austral Yungas (Ministerio de
Ambiente y Desarrollo Sostenible & Sociedad Argentina para el Estudio de los Mamíferos, ; Fig. ), with the species group for those
species included in our analysis (i.e. small mammals, large herbivores, species of conservation concern and felids), national and IUCN Red
List status for native species, and whether or not recorded in our camera-trap study during –. The table does not include uniden-
tified small mammal species.
National Native/
Species (by family) Species group status1 Red List status2 exotic Recorded
Didelphidae
White-eared oposum Didelphis albiventris LC LC Native Yes
Thick-tailed oposum Lutreolina massoia NT LC Native Yes
Mymercophagidae
Southern tamandua Tamandua tetradactyla NT LC Native Yes
Giant anteater Myrmecophaga tridactyla VU VU Native Yes
Dasypodidae
Armadillo Dasypus mazzai DD DD (as Dasypus Native No
yepesi)
Nine-banded long-nosed armadillo Dasypus LC LC Native No
novemcinctus
Six-banded armadillo Euphractus sexcinctus LC LC Native Yes
Cebidae
Brown capuchin monkey Sapajus cay VU LC Native Yes
Canidae
Crab-eating fox Cerdocyon thous LC LC Native Yes
Pampas fox Lycalopex gymnocercus LC LC Native Yes
Domestic dog Canis lupus Exotic Yes
Felidae
Jaguarundi Herpailurus yagouaroundi Felid LC LC Native Yes
Pampas cat Leopardus colocolo Felid VU NT Native Yes
Geoffroy’s cat Leopardus geoffroyi Felid LC LC Native Yes
Oncilla Leopardus tigrinus Felid VU VU Native Yes
Ocelot Leopardus pardalis Felid VU LC Native Yes
Margay Leopardus wiedii Felid VU NT Native Yes
Cougar Puma concolor LC LC Native Yes
Jaguar Panthera onca Conservation CR NT Native Yes
concern
Domestic cat Felis catus Exotic No
Mustelidae
Molina’s hog-nosed skunk Conepatus chinga LC LC Native Yes
Neotropical river otter Lontra longicaudis NT NT Native No
Tayra Eira barbara NT LC Native Yes
Little grison Galictis cuja LC LC Native Yes
Procyonidae
Crab-eating raccoon Procyon cancrivorus LC LC Native Yes
South American coati Nasua nasua LC LC Native Yes
Tapiridae
Lowland tapir Tapirus terrestris Conservation VU VU Native Yes
concern
Tayassuidae
Collared peccary Pecari tajacu VU LC Native Yes
White-lipped peccary Tayassu pecari Conservation EN VU Native Yes
concern
Cervidae
Red brocket deer Mazama americana Herbivore VU DD Native Yes
Gray brocket deer Mazama gouazoubira Herbivore LC LC Native Yes
Leporidae
Tapeti Sylvilagus brasiliensis Small mammal LC EN Native Yes
Common hare Lepus europaeus Exotic No
Sciuridae
Yungas squirrel Sciurus ignitus Native Yes
Oryx, 2022, 56(6), 877–887 © The Author(s), 2022. Published by Cambridge University Press on behalf of Fauna & Flora International doi:10.1017/S0030605321001538
https://doi.org/10.1017/S0030605321001538 Published online by Cambridge University PressEffect of free-ranging cattle on mammalian diversity 881
TABLE 1 (Cont.)
Species (by family) Species group National Red List status2 Native/ Recorded
status1 exotic
Erithizontidae
Bicolored-spined porcupine Coendou bicolor VU LC Native No
Prehensile-tailed porcupine Coendou prehensilis VU LC Native No
Hydrochaeridae
Capybara Hydrochoerus hydrochaeris LC LC Native No
Dasyproctidae
Yungas agouti Dasyprocta sp. Small mammal LC LC Native Yes
Myocastoridae
Coypu Myocastor coypus LC LC Native No
Suidae
Pig Sus scrofa Exotic Yes
Bovidae
Cattle Bos taurus Exotic Yes
Equidae
Horse Equus caballus Exotic Yes
Donkey Equus asinus Exotic Yes
Ovidae
Sheep Ovis aries Exotic Yes
Capridae
Goat Capra sp. Exotic Yes
Ministerio de Ambiente y Desarrollo Sostenible & Sociedad Argentina para el Estudio de los Mamíferos ().
IUCN ().
DD, Deficient Data; LC, Least Concern; NT, Near Threatened; EN, Endangered; CR Critically Endangered.
index (RAI) as: abundance, primary production and the human influence
index; for species of conservation concern: cattle abun-
RAIi = ntot/daystot × 100 (1) dance, primary production, human influence index, land
where ntot is the number of independent events of the ith protection status and distance to water lines; for the felid
species and daystot is the total number of effective trap- community: cattle relative abundance index and the
nights, using the package camtrapR (Bengsen et al., ; human impact index. For presence/absence models, we
Mandujano & Pérez-Solano, ) in R .. (R Core used the negative binomial error and Gaussian distributions
Team, ). We calculated two measures of diversity, for abundance, using the package MASS (Venables & Ripley,
using the package vegan (Oksanen et al., ) in R: species ) in R. We checked for homogeneity by plotting resi-
richness (S) and the Shannon–Weaver index (H). The latter duals vs fitted values, for normality using quantile-quantile
was calculated as: plots, and for independence by plotting residuals vs each ex-
planatory variable. Because we had several combinations of
S
H=− RAI i × ln(RAI i ) (2) variables and therefore multiple models, we used single-
i=1
term deletions to obtain the most parsimonious model,
The value of the relative abundance index increases with in- using Akaike’s information criterion (AIC; Burnham &
creasing richness and evenness in the abundance of species Anderson, ).
in the community.
We developed generalized linear models (GLM) to
examine the effect of cattle and land protection status on A niche-based model for cattle
S and H. As biodiversity follows global patterns, with an in-
crease in species richness toward the tropics and a decline in Species distribution models examine the potential influence
species richness with increasing elevation (Pianka, ; of environmental variables on species presence. MaxEnt
Lomolino, ; Hillebrand, ), we included altitude finds the distribution of maximum entropy (i.e. the largest
and latitude as factors in the models. For each of the four spread in a geographical dataset of species presences), sub-
species groups we examined the potential influence of ex- ject to the constraint that the projected value of each variable
planatory variables on presence/absence of species and on is close to its empirical average (Phillips et al., ). This
relative abundance index; for small mammals: cattle abun- information can then be extrapolated to non-sampled
dance and primary production; for large herbivores: cattle areas (Phillips et al., ).
Oryx, 2022, 56(6), 877–887 © The Author(s), 2022. Published by Cambridge University Press on behalf of Fauna & Flora International doi:10.1017/S0030605321001538
https://doi.org/10.1017/S0030605321001538 Published online by Cambridge University Press882 G. A. E. Cuyckens et al.
FIG. 2 Mean native species richness recorded by camera traps set
in areas of varying protection status. Boxes represent the
interquartile range, box widths are proportional to the square
root of the sample sizes, the horizontal solid line indicates the FIG. 3 Habitat suitability for cattle Bos taurus (from the
median, and the whiskers indicate the % CI. niche-based model) in relation to the human influence index.
The study area for modelling was the Yungas ecoregion recorded by (%) cameras. Gray brocket deer had a
with a -km buffer. We generated , random points relative abundance index of –, and red brocket deer
to extract values for the environmental variables, and tested –. Among the species of conservation concern, the
for correlations with the Pearson test, selecting only those lowland tapir had the highest relative abundance index (re-
with a correlation # .. These were: mean diurnal tem- corded by cameras), the white-lipped peccary had the
perature range, temperature seasonality, mean temperature lowest relative abundance index (three cameras) and the jag-
of wettest quarter, precipitation of driest quarter, precipita- uar was recorded by cameras. The ocelot was the most
tion of warmest quarter, roughness, human influence index, abundant felid species, followed by the margay, jaguarundi,
and distance to nearest water lines. oncilla, Pampas cat and Geoffroy’s cat. The maximum num-
We used presence records of cattle obtained from the ber of small and medium-sized felid species detected by one
camera traps. We ran the species distribution model camera was five.
times and used the average outcome. To measure the general Native species richness was almost % higher in nation-
performance, we used the area under the receiver operating al parks and private protected areas than in provincial
characteristic curve (AUC), which measures the probability protected areas, with intermediate values for Indigenous
that a randomly chosen presence point will rank above a territories and private lands (Fig. ). Native species richness
randomly chosen background point (AUC . = random; and diversity decreased with altitude, without interactions
values closer to indicate better discrimination power; with cattle relative abundance index or latitude (Fig. ,
Bellamy et al., ). We converted the model into a binary Table ).
model by applying the minimum presence logistic threshold Presence, but not relative abundance, of small mammals
(.) and categorized habitat suitability for cattle into five and large native herbivores was influenced by cattle relative
classes (very low: , .; low: .–.; medium: .– abundance index. For small mammals to be present, the
.; high: .–.; very high: ˃ .) for visualization as relative abundance index of cattle had to be , , and large
a map. herbivores were absent at a cattle relative abundance index
of and present at . Thus, to assure the presence of large
herbivores, the number of independent cattle records
Results should not be greater than five times the number of effective
trap-nights (for example, in a survey of trap-nights the
We recorded native species, % of the species that could number of independent cattle events should be , ).
potentially occur in the region (Table ), and seven exotic Lowland tapir relative abundance increased with distance
species, with of cameras (%) recording at least from water lines and was not influenced by cattle relative
one native species and cameras (%) at least one exotic abundance index. Jaguar relative abundance and presence
species. The range of species richness per camera was – were not significantly associated with any of the measured
(mean .) for native and – (mean .) for exotic species. variables. Data for the white-lipped peccary could not be
Bos taurus had the highest relative abundance index and was analysed because there were only three records. The
also the most frequently recorded species. Other domestic human influence index negatively affected felid richness,
species recorded were horses, pigs, goats and dogs. but not relative abundance, with an abrupt decrease in rich-
Domestic cats were not recorded. ness at a human influence index of $ . Primary produc-
Small mammals were recorded by cameras (%). tion did not influence the presence or relative abundance of
Brocket deer (i.e. M. gouazoubira or M. americana) were small mammals or the tapir (Table ).
Oryx, 2022, 56(6), 877–887 © The Author(s), 2022. Published by Cambridge University Press on behalf of Fauna & Flora International doi:10.1017/S0030605321001538
https://doi.org/10.1017/S0030605321001538 Published online by Cambridge University PressEffect of free-ranging cattle on mammalian diversity 883
TABLE 2 Generalized linear models for native species richness absent where the cattle relative abundance index was
(number of species) and diversity (Shannon−Weaver index), above and , respectively. Felids were negatively affected
small mammal presence/absence, deer Mazama sp. presence/ab- by the human influence index but not by cattle relative
sence, lowland tapir Tapirus terrestris relative abundance index
abundance, suggesting that felids are influenced not by cat-
and felid species richness in the Austral Yungas. Only significant
models are presented, with t and P values for potentially influential
tle directly but by activities related to their presence. As cat-
variables. tle have the potential to inhabit most of the Austral Yungas
and their presence is associated with hunting, exotic species
t P (domestic dogs and cats), and selective logging (Perovic,
Species richness ), we recommend cattle should be reduced to abun-
Latitude 0.036 0.846 dances that allow coexistence with wildlife in all areas
Altitude −0.002 0.0002** with forest cover, and excluded from strictly protected
Protection status −0.850 2.75 × 10−08**
Cattle relative abundance index −0.005 0.415
areas. Strictly protected areas (private or state-managed)
Species diversity are the only management regime ensuring long-term
Latitude 0.060 0.197 fauna conservation in the Yungas.
Altitude −4.96 × 10−04 1.54 × 10−06** We recorded % of the native species that could poten-
Land protection status −0.123 0.001* tially occur in the Austral Yungas and therefore we consider
Cattle relative abundance index −0.002 0.239 our methodology successful. We did not record water-
Small mammals associated species such as the capybara Hydrochoerus hy-
Cattle relative abundance index −2.100 0.041*
drochaeris, nutria Myocastor coypus and neotropical otter
Primary productivity −0.078 0.938
Deer Lontra longicaudis, the latter being rare in the Yungas
Cattle relative abundance index 0.023 0.021* (Albanesi et al., ). As we did not place cameras in trees,
Human influence index 1.859 0.067 our methodology was not suitable for detecting arboreal
Tapir relative abundance index species such as the bicolored-spined porcupine Coendou
Cattle relative abundance index −0.039 0.781 bicolor and prehensile-tailed porcupine Coendou prehensi-
Primary productivity 0.937 0.352 lis, which are also rare. We did, however, record arboreal
Distance to rivers 2.070 0.042*
species such as the capuchin monkey Sapajus cay and
Felid species richness
Cattle relative abundance index −0.814 0.418 Bolivian squirrel Sciurus ignitus, but on the ground. Only
Human influence index −2.870 0.005* two of the six cingulate species (armadillos) were recorded,
suggesting they have a naturally low relative abundance or
*P , .; **P , ..
are difficult to record with camera traps. A national-scale as-
sessment indicated the need to protect these six species
We obtained a habitat suitability model for cattle with (Abba et al., ).
AUC = .. Values . . are considered to indicate mod- The niche-based distribution model for cattle shows their
els with a good general performance (Phillips & Dudík, potential to occupy almost the entire Yungas ecoregion ex-
). Cattle encounter suitable habitat in most (%) of cept for the mountain peaks, probably because of the low
the Yungas, with higher habitat suitability towards lower la- winter temperatures, low carrying capacity and the difficulty
titudes and lower suitability towards higher altitudes of access for people. The positive association between habi-
(Fig. ). Habitat suitability for cattle increases with the tat suitability for cattle and the human influence index is a
human influence index, peaking at and then decreasing result of the association of cattle with people, but areas with
abruptly (Fig. ). Lower suitability corresponds to areas al- a human influence index ˃ are no longer suitable for cat-
ready transformed into croplands, human settlements or tle. The raster layer of suitable habitat for cattle could be
roads (Fig. ). used in areas not surveyed to estimate cattle presence locally,
and could serve as a tool to analyse the effects of cattle in the
Austral Yungas.
Discussion Environmental variables, which are influenced by lati-
tude and altitude, affect the diversity and composition of
As far as we are aware, this is the first study to use a large native biodiversity. As predicted, we found a decrease in
camera-trap data set for the Yungas ecoregion over an ex- species richness and diversity with an increase in elevation,
tended period ( years) and the first to examine the factors in accordance with global patterns (Lomolino, ) and
affecting the native mammalian community. In contrast to with a previous study in the northern Yungas (Di Bitetti
our expectation, general mammalian species richness and et al., ). We found high mountain areas in the Yungas
diversity were not directly related to the cattle relative abun- to be naturally poorer in native and exotic species than for-
dance index, but the latter affected two of the four groups of ests at lower elevations. The northern Austral Yungas has
species studied. Small mammals and brocket deer were higher species richness than the central and southern
Oryx, 2022, 56(6), 877–887 © The Author(s), 2022. Published by Cambridge University Press on behalf of Fauna & Flora International doi:10.1017/S0030605321001538
https://doi.org/10.1017/S0030605321001538 Published online by Cambridge University Press884 G. A. E. Cuyckens et al.
FIG. 4 Presence records of cattle
with (a) predicted habitat
suitability (see text for details),
and (b) the human influence
index (see text for details) in the
Austral Yungas of Argentina.
), depending on their management. National Parks in
Argentina are legally required to exclude cattle, although
this regulation is not always implemented. They are gener-
ally larger and have stricter controls than provincial and pri-
vate protected areas and have historically been established
in areas with low potential for economic development
(Margules & Pressey, ; Rodrigues et al., ), and
hence could have a higher intrinsic value for conservation.
Thus, various anthropogenic factors seem to be implicated
in the persistence of native large mammals in these areas.
FIG. 5 Native species richness per camera trap in relation to Indigenous territories, with intermediate cattle abundance,
elevation during an -year camera-trap study in the Austral may contribute to conservation and offer a complementary
Yungas of Argentina. institutional model to state-run protected areas (Johnson &
Nelson, ). Provincial protected areas, with higher cattle
Austral Yungas and is the southern limit of the distributions relative abundance index, had the lowest diversity indices,
of several mammal species (Sapajus cay, Tapirus terrestris, similar to unprotected areas (private or state property). In
Leopardus wiedii), emphasizing the role of this part of the low-income countries, nature conservation is not neces-
ecoregion in the conservation of these species. In contrast sarily a priority and so-called paper parks (i.e. protected
to general patterns (Brown & Lomolino, ) and to areas that only exist on paper and do not achieve conserva-
those of small forest mammals in the Yungas (Ojeda et al., tion goals), are common (Rodríguez & Rodríguez-Clark,
), we found that latitude did not influence native spe- ). Nevertheless, even paper parks matter (Rodríguez &
cies richness and diversity, indicating a latitudinally homo- Rodríguez-Clark, ) if they still have forest cover. To re-
genized native mammal community. verse the failure in the achievement of conservation objec-
Land protection status was the most important variable tives of such paper parks in Argentina and to achieve
in explaining native mammalian biodiversity. We recorded conservation goals, we recommend lowering cattle relative
the highest values of native species richness and diversity in abundance index to # (the highest limit compatible with
national parks, highlighting the importance of strictly pro- the presence of both deer and small mammals) and estab-
tected areas and the complementary role of small private lishing adaptive management plans that include stricter
protected lands (Johnson & Nelson, ; Kamal et al., controls than at present.
Oryx, 2022, 56(6), 877–887 © The Author(s), 2022. Published by Cambridge University Press on behalf of Fauna & Flora International doi:10.1017/S0030605321001538
https://doi.org/10.1017/S0030605321001538 Published online by Cambridge University PressEffect of free-ranging cattle on mammalian diversity 885
Our findings indicate that high cattle abundance (relative cattle and human activities such as habitat destruction and
abundance ˃ ) is incompatible with the presence of small hunting for food (peccaries) and in retaliation (jaguars), are
mammals. Trampling and browsing by cattle reduce the het- probably having negative, synergistic effects on species of
erogeneity of the forest understorey for this group (Smith conservation concern (Romero-Muñoz et al., ). These
et al., ; Hayward et al., ). We could not identify species depend on protected forests with extensive cover
small mammals to species level and the responses of indi- and protection against hunting.
vidual species to cattle may vary (Schieltz & Rubenstein, This is the first study based on an extensive camera-trap
). Nevertheless, when present, small mammals had high survey to provide evidence that cattle affect the assemblage
relative abundance indices, so a prey base for medium-sized of mammals in the Austral Yungas, both directly and indir-
and small felids remains available. ectly. We have provided guidelines for cattle abundance that
Small felids are indirectly affected by cattle, as indicated should be implemented in protected areas where cattle rais-
by the human influence index. This index includes human ing is allowed. However, we cannot provide guidelines for
population pressure, human land use and infrastructure and cattle abundance compatible with species of conservation
human access. Differential logging (i.e. logging of only par- concern (jaguar and white-lipped peccary), and their low
ticular tree species and individuals of a certain size, resulting abundances indicate their high risk of extinction in this
in impoverished species richness and affecting forest struc- region. Following Mazzini et al. (), we used directly
ture) could also affect forest specialists such as the oncilla measured cattle relative abundance at the local scale and
and margay. Therefore, we suggest direct hunting and asso- complemented this with an indirect method at the regional
ciated activities, such as the presence of dogs (Perovic, ) scale (distribution modelling). Our work therefore provides
and habitat transformation, are underlying explanations for both a method for future assessments of cattle impacts and
the influence of humans on felids, not the presence of cattle an indicator of potential cattle abundance in unsurveyed
directly. We did not record domestic cats, so these may not areas in the Austral Yungas.
yet be a threat to small felids in the Yungas. We found that
the Vulnerable oncilla had the lowest relative abundance Acknowledgements We thank all field assistants and landowners
who allowed us to conduct fieldwork, the Tinkunaku community,
and was the rarest of the felid group and therefore its con- park rangers of the Secretariat of Environment and Sustainable
servation status should be monitored. Development of Salta province, the National Park Administration of
In agreement with Nanni (), we found brocket deer Argentina; IDEA WILD for providing equipment; Leonidas
only in areas with low cattle relative abundance. The human Lizarraga for help downloading data; Agustin Abba for assistance
influence index did not affect these large herbivores, sug- with identification of ungulates; Tadeu de Oliveira for help with iden-
tification of small felids; two anonymous reviewers for advice; and
gesting a direct effect of cattle on these two species. In agree-
Martin Fisher and the teachers and classmates of the Conservation
ment with Mazzini et al. (), we suggest biological inter- Leadership Programme Writing for Conservation Course in Colombia.
actions such as competition and dietary overlap between
cattle and native herbivores are the cause of this effect. Author contributions Study conception: GAEC, LRM; study de-
Species of conservation concern had low relative abun- sign, fieldwork: GAEC, PGP; data input: GAEC, NGBT; data analysis:
GAEC, writing: all authors.
dance indices. Lowland tapir relative abundance was nega-
tively influenced by distance to linear watercourses. Like the Conflicts of interest None.
Malayan tapir Tapirus indicus and Baird’s tapir Tapirus
baardii, which depend on proximity to water (Dudgeon, Ethical standards This research abided by the Oryx guidelines on
; Reyna-Hurtado et al., ), lowland tapirs use ethical standards.
water banks to browse and mate, and enter the water to
take refuge from predators (Brooks et al., ). Lowland
tapir relative abundance was not negatively influenced by References
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