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Mammalia 2015; 79(1): 115119

Short Note
Alexandra Pineda-Guerrero, Jos F. Gonzlez-Maya* and Jairo Prez-Torres

Conservation value of forest fragments for


medium-sized carnivores in a silvopastoral
system in Colombia
Abstract: Silvopastoral cattle ranching is seen as a viable
land use management system, which unlike traditional
land use systems preserve forested areas and prevent loss
of important habitats for carnivores. We evaluated carnivore abundance and habitat use in a 50-year silvopastoral system located in the Cordoba department, Caribbean
region of Colombia. Transects and track plots were established both in forest fragments and pastures within the silvopastoral system and were sampled for carnivore signs.
Crab-eating raccoon, Crab-eating fox, and Gray fox were
the most abundant species and showed higher preference
for forest than pastures. Our results reflect the importance
of forest cover within livestock systems and highlight the
potential of these land use systems for carnivore and tropical dry forest conservation in fragmented landscapes.
Keywords: abundance; carnivores; habitat use; livestock,
silvopastoral.
DOI 10.1515/mammalia-2013-0050
Received March 25, 2013; accepted April 15, 2014; previously
published online May 9, 2014

Tropical dry forests (TDFs) are one of the most threatened


forest types in the world and have suffered severe transformations in the last decade due to unsustainable forest

*Corresponding author: Jos F. Gonzlez-Maya, The Sierra to Sea


Institute/ProCAT Colombia, Calle 127 # 45-76, Bogot, Colombia;
and Laboratorio de Ecologa y Conservacin de Fauna Silvestre,
Instituto de Ecologa, Universidad Nacional Autnoma de Mxico,
Mexico, e-mail: jfgonzalezmaya@gmail.com
Alexandra Pineda-Guerrero: Pontificia Universidad Javeriana,
Facultad de Ciencias, Departamento de Biologa, Unidad de Ecologa
y Sistemtica (UNESIS), Laboratorio de Ecologa Funcional, Bogot,
Colombia; and The Sierra to Sea Institute/ProCAT Colombia, Calle
127 # 45-76, Bogot, Colombia
Jairo Prez-Torres: Pontificia Universidad Javeriana, Facultad de
Ciencias, Departamento de Biologa, Unidad de Ecologa y Sistemtica
(UNESIS), Laboratorio de Ecologa Funcional, Bogot, Colombia

logging, extensive cattle farming, and agriculture (Miles


etal. 2006, Dirzo etal. 2011). Colombia has an important
network of TDFs with a significant number of endemic
species, which are currently under high levels of threat
and poorly represented in protected areas (Dirzo etal. 2011,
Rodriguez etal. 2012). The Caribbean region of Colombia
contains the highest proportion of unprotected TDF in
the country (Gonzlez-Maya et al. 2010), and although
they have suffered extensive deforestation processes and
cattle ranching, the remnants still provide potential habitats for many species, particularly carnivores (GonzlezMaya etal. 2013). Given the importance and severe threats
toward TDFs, alternative land use management strategies
may need to be implemented on private productive lands
to conserve them (Murgueitio etal. 2011). These alternatives could provide an opportunity for the maintenance of
biodiversity in fragmented regions, providing habitat, key
resources, and connectivity for populations (Daily et al.
2003, Chacn and Harvey 2008). Silvopastoral systems, in
which trees and livestock are managed on the same land
unit, were proposed to improve both productivity and
conservation values of the land (Pezo and Ibrahim 1998).
This contributes to the conservation objectives of a region
by providing habitat for many native species and connecting forest remnants (Chacn and Harvey 2008) and by
providing tree cover in the form of forest fragments, live
fences, isolated trees in pastures, and windbreaks (Pezo
and Ibrahim 1998). The implementation of silvopastoral
systems in Colombia has resulted in significant advances
to land use systems in terms of sustainable production
and ecosystem services (Crdenas etal. 2000, Vallejo etal.
2012). However, it is not yet known what impact this land
use system has on the maintenance of biodiversity, and
especially on carnivores, as well as the preservation of the
TDF ecosystem, itself. The objective of our study was to
evaluate the conservation value of forest patches within
silvopastoral systems for carnivores by examining carnivore habitat use and abundance within pasture and forest
fragments.

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116A. Pineda-Guerrero etal.: Carnivores in silvopastoral systems


The study was conducted in the department (province) of Crdoba, located in Northwestern Colombia,
within the Caribbean region of the country. The department has a long history of environmental degradation
where most ecosystems have been transformed into
anthropogenic savannas as a result of the unplanned agriculture and livestock production (Gonzlez-Maya et al.
2013). The study site is located within Betanc-Guacamayas (81118N, 753249W) a 460-ha private farm located
in the Buenavista area, north of the Western Andes Mountain range (70 m asl, Temp. 28C; Figure 1). The farm is
entirely dedicated to livestock production in a silvopastoral land use system, preserving forest remnants, gallery
forest, and planting native trees to connect existing forest
remnants. Managed pastures are characterized by three
introduced grass species (Brachiaria humidicola, Brachiaria decumbens, and Brachiaria dyctioneura) as well as
native pasture species.
We evaluated the carnivore assemblage within the
TDF fragments and pasture land using two complementary methodologies: line transects and track plot stations. The total sampling area was 60.57 ha, 46.85% of
which corresponds to forest fragments and 53.15% corresponds to pastures. Sampling was conducted during
rainy season between June and July 2010. All tracks were
identified including standard measurements (Aranda
2000). We surveyed three transects within forest fragments
(0.830.19 km) and three within pasture patches
(0.830.45 km), all organized and distributed along the
entire study site avoiding pseudo-replicates (Figure 1). All
transects were sampled daily between 6h30 and 17h30.
Carnivore presence was counted based on footprints,

Figure 1Study area and selected forest patches and pastures for
carnivore surveys with transects and track plots in a silvopastoral
system in a tropical dry forest of Crdoba department, Colombia.

feces, burrows, hairs, visual sightings, and any other signs


of species presence; we ensured no double counts of the
same signs. Additionally, 100 track plot stations with an
area of 1m2 (50 in the forest and 50 in pasture) were established. These were covered with sieved sand and baited
with visual (chicken feathers) (Long etal. 2008) and olfactory (rotten eggs with flour, sardines, and dog food with
chicken flavor and cod liver oil) attractants. Each plot was
placed 10m left or right of the transect and were spaced
50 m apart from each other. Relative abundance indices
were calculated for both methodologies (transects and
track plots) independently, using the number of carnivore
track encounters per sampling unit. Transects and track
plot data were used to estimate carnivore relative abundance as tracks per km (t/km) and visits to plots per total
active plots multiplied by 100 (pt/ap), for both forest and
pasture areas, respectively (Carrillo et al. 2000). Habitat
use was evaluated only with transect data as the total
number of tracks per species for each land cover normalized by distance surveyed. A Chi square test was used to
test for differences between the two land covers (Lovallo
and Anderson 1996). If differences were found, the proportion of tracks per species was calculated for each land
use with Bonferroni 95% confidence intervals. Speciesspecific selection or avoidance of each land use was determined by comparing the proportion used against that
available within the study area. The expected values were
calculated by multiplying the ratio of cover area with the
number of tracks that were encountered for each land use
type.
A total of 1018 footprints, four direct sightings, and
seven fecal samples were obtained belonging to seven
carnivore species of four families. Among these, two canid
species [crab-eating fox Cerdocyon thous (Linnaeus, 1766)
and gray fox Urocyon cinereoargenteus (Schreber, 1775)],
two felids [Ocelot Leopardus pardalis (Linnaeus, 1758)
and Margay Leopardus wiedii (Schinz, 1821)], two mustelids [Neotropical Otter Lontra longicaudis (Olfers, 1818)
and long-tailed weasel Mustela frenata (Lichtenstein,
1831), and one procyonid (crab-eating raccoon Procyon
cancrivorus (G. [Baron] Cuvier, 1798)] were identified. We
obtained a higher detection of carnivores in transects
compared with track plots. According to the track plots
visited by carnivores, the scent that attracted the most carnivores was chicken-flavored dog food with cod liver oil
(78.95%), while rotten eggs with flour and sardine scent
attractants were less effective (10.53% each). The relative abundance of the total carnivore assemblage for the
forest cover (47.36 t/km) was significantly higher than the
pasture cover (2.60 t/km), for a total relative abundance
of 49.96 t/km inside the silvopastoral livestock system.

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A. Pineda-Guerrero etal.: Carnivores in silvopastoral systems117

Table 1Carnivore relative abundance estimated by transects and


track plots in forest and pastures in a silvopastoral system in a
tropical dry forest of Crdoba department, Colombia.
Species

Procyon cancrivorus

Cover type

Transect
(t/km)

Track plot
(pt/ap)

20.64
0.8
12.28
1.4
8.24
0.4
5.64
0.32
0.24
0.04

0.6
Not detected
0.2
0.2
0.3 pt/ap
0.4 pt/ap
Not detected
0.1
Not detected
Not detected

Cerdocyon thous

Urocyon cinereoargenteus

Lontra longicaudis

Leopardus pardalis

Mustela frenata

Leopardus wiedii

Forest
Pastures
Forest
Pastures
Forest
Pastures
Forest
Forest
Forest
Forest

Relative abundance

t/km, tracks/km; pt/ap, visits to plots/total active plots.

P. cancrivorus and C. thous were always more abundant


in forest than pastures with both methods. L. longicaudis,
L. pardalis, and M. frenata were detected only in forests,
but both L. pardalis and M. frenata occurred in relatively
lower abundance than L. longicuadis. U. cinereoargenteus
was more abundant in forests by transect method, but
was less abundant by track plots (Table 1). L. wiedii was
only detected once and thus was not used for analyses.
P. cancrivorus (2=612.48, p<0.05, df=2, n=536), C. thous
(2=300.73, p<0. 05, df=2, n=342), and U. cinereoargenteus
(2=238.52, p<0.05, df=2, n=216) showed the higher relative abundance values in the forest area compared to the
pasture area with transect data. All three species showed
higher preference for forest areas over pastures (Figure 2).
We found that generalist species were detected in both
pasture and forest fragments, but were significantly more
abundant in forests. By contrast, specialists were never
detected in pastures. Some species present in the area such

P. cancrivorus

1
Bonferroni intervals
(probability)

as Conepatus semistriatus, Eira barbara, Galictis vittata,


Puma yagouarondi, Puma concolor, Panthera onca, Nasua
nasua, and Speothos venaticus (Solari etal. 2013) were not
found in our study; it is likely that forest reduction and
hunting may have caused severe population reduction,
and even local extinctions, in this fragmented landscapes
(Gonzlez-Maya etal. 2013). Our results support previous
findings that generalist species, such as Procyon cancrivorus, Cerdocyon thous, Urocyon cinereoargenteus, and
Leopardus pardalis, are more abundant in transformed
landscapes and use forest and pastures as refuge, preferring forested areas (Michalski and Peres 2005, SnchezLalinde and Prez 2008, Di Bitetti et al. 2009), whereas
more specialist species, such as Leopardus weidii, Lontra
Longicaudis, and Mustela frenata, are uncommon in such
landscapes because they require high-quality habitat and
have specific refuge requirements, such as shelter trees
and, in the case of the Neotropical otter, require riverbanks with adequate escape cover (Emmons 1990, Reid
1997, Devenish and Sayer 2007).
These results demonstrate the importance of conserving and connecting forest fragments for these rare
carnivore species with low ability to use the matrix and
surrounding resources. Forest fragments are the only
habitat available in the landscape for rare species, and
pastures may be an inhospitable matrix that is impermeable to some species limiting their connectivity. In
landscapes with highly fragmented habitats, the spatial
arrangement of habitat patches is very important, and
ecological generalists should benefit from environments
that are heterogeneous and be more common, whereas
ecological specialists are expected to benefit from environments that are relatively homogeneous (Andren 1994,
Marvier et al. 2004, Devictor et al. 2008). Forest fragments may be fundamental to maintain both generalist
and rare carnivore species; despite some species will be

C. thous

0.8

U. cinereoargenteus

0.6
0.4
0.2
0

Exp.

Obs.

Exp.

Obs.
Pasture

Forest
Cover

Figure 2Comparison of habitat use (proportion of tracksBonferroni 95% confidence intervals) by three species of carnivores with habitat
available estimated by transects and track plots in forest and pastures in a silvopastoral system in a tropical dry forest of Crdoba department, Colombia.

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118A. Pineda-Guerrero etal.: Carnivores in silvopastoral systems


more restricted to the forest patches, our data and previous works suggests that even generalists require forest
for some biological and ecological requirements. Further
exploration is needed to certainly assess to what extent
source-sink dynamics model species assemblages and
how forests represent the necessary habitat for population
maintenance.
TDFs have suffered significant reductions in the
Crdoba department due to unsustainable livestock
management, resulting in many small forest remnants
with low connectivity (Gonzlez-Maya et al. 2013). This
extensive disturbance have affected carnivore assemblages, first extirpating top predators, such as jaguar and
puma, probably generating trophic cascades (Estes etal.
2011) and, second, isolating populations to the forest
islands embedded on pasture matrices (Prist etal. 2012).
This isolation has significant impacts on population
viability, gene flow, and other fundamental population
aspects (Laurance et al. 2011), and thus, maintaining
and promoting connectivity is a priority to restore large
mammal assemblages in fragmented landscapes (Prist
etal. 2012). The results of our study indirectly reinforces
that silvopastoral systems represent a more appropriate system to maintain biodiversity than conventional
or extensive pasture systems, and its implementation
could be considered an advance in halting the ongoing
destruction of ecosystems. Current configuration of the
Caribbean landscapes, pastures matrices with forest
fragments, could be the basis for conservation under a
silvopastoral framework, where fragments should be
prioritized for incentives for their maintenance. Previous studies have shown a significant improvement in the
conditions of biodiversity when sustainable silvopastoral systems are established (Tobar and Ibrahim 2009).
Our finding provides some preliminary results on carnivore assemblages and habitat use in these systems. As
most of current landscapes have been disturbed in the
Neotropical region for human use, it is considered that
the future of biodiversity rely in these human-dominated
areas (Daily et al. 2003), therefore, understanding how
specific groups respond to disturbance and how sustainable land use contributes to biodiversity should be
the research priority for conservation biology. The takehome message of this study is not only the importance of
TDFs as natural habitat for carnivores but also show that
pastures alone do not provide the necessary conditions
for these species. As the official protected areas system
still do not cover a significant proportion of TDFs in the
country, private initiatives should be promoted in order
to improve biodiversity well-being.

Acknowledgments: We would like to thank E. Payn, T.


Boorsma, and I. Vela-Vargas for reviewing the project and
manuscript in its early stages. This project was partially
funded by R. Escobar and P. Betancourt from the Hacienda Betanc-Guacamayas and the Functional Ecology
Laboratory (Universidad Javeriana). Thanks to A. Mejia,
S. Gmez, G. Jimenez, and J. Ballesteros, for their support
and help during the field stage.

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