PBPrimate BiologyPBPrimate Biol.2363-4715Copernicus PublicationsGöttingen, Germany10.5194/pb-4-61-2017Report on the presence of a group of golden-headed lion tamarins
(Leontopithecus chrysomelas), an endangered
primate species in a rubber plantation in southern Bahia, BrazilDe VleeschouwerKristel M.kristel.devleeschouwer@kmda.orgOliveiraLeonardo C.Centre for Research and Conservation, Royal Zoological Society of
Antwerp, 2018 Antwerp, BelgiumDepartamento de Ciências, Faculdade de Formação de
Professores, UERJ, CEP 24435-005, São Gonçalo, RJ, BrazilPrograma de pós-graduação em Ecologia e
Conservação da Biodiversidade, Universidade Estadual de Santa Cruz,
UESC, Salobrinho, CEP 45662-900, Ilhéus, BA, BrazilBicho do Mato Instituto de Pesquisa, CEP 30360-082, Belo Horizonte,
MG, BrazilKristel M. De Vleeschouwer (kristel.devleeschouwer@kmda.org)14March201741616722December201614February201720February2017This work is licensed under a Creative Commons Attribution 3.0 Unported License. To view a copy of this license, visit http://creativecommons.org/licenses/by/3.0/This article is available from https://pb.copernicus.org/articles/4/61/2017/pb-4-61-2017.htmlThe full text article is available as a PDF file from https://pb.copernicus.org/articles/4/61/2017/pb-4-61-2017.pdf
In a landscape fragmented by agriculture, the extent to
which forest-dwelling primates can use the matrix between fragments can be
critical for their long-term survival. So far, the golden-headed lion
tamarin (Leontopithecus chrysomelas), an endangered primate inhabiting the Atlantic Forest of
south Bahia, is only known to use shaded cacao (Theobroma cacao)
agroforests within the
matrix. We report on the use of a rubber plantation by a group of
golden-headed lion tamarins between August 2013 and January 2014. The
group used the rubber plantation on 16 of the 22 observation days (73 %),
and we recorded behaviours such as eating, grooming and sleeping, consistent
with the use of the area as a home range. We also observed associations with
Wied's marmosets (Callithrix kuhlii). The locations of group sightings were not
uniformly spread across the entire area of the rubber plantation, suggesting
preferred use of certain areas. The presence of resources such as jackfruits
(Artocarpus heterophyllus) and epiphytic bromeliads may be attracting both species to these
plantations. In addition to shaded cacao plantations, rubber plantations
with the appropriate structure may be a viable option for increasing forest
connectivity for both species in south Bahia, reconciling economic rubber
production with primate conservation.
Introduction
The conversion of forests for agriculture is a major cause of tropical forest
fragmentation and degradation (Gibbs et al., 2010). The resulting landscape
of smaller forest fragments embedded within a generally inhospitable matrix
represents particular challenges to animals, especially rendering
matrix-intolerant species more vulnerable to extinction (Benchimol and
Peres, 2014). Matrix permeability critically determines dispersal between
fragments, which in turn is essential for maintaining a sufficient level of
gene flow and genetic diversity among small fragmented populations (Donald
and Evans, 2006).
Representative images of the rubber plantation (Photos: Kristel De
Vleeschouwer).
Forest-dwelling primates are particularly sensitive to the effects of
anthropogenic forest fragmentation, with many species experiencing
population decline or extinction (Benchimol and Peres, 2014). Loss of
habitat due to agricultural expansion is the principal threat to primate
populations worldwide, with livestock farming and ranching constituting the
second most important threat in the Neotropics (Estrada et al., 2017). Yet
high human population growth and poverty rates in primate-range countries,
as well as global market economics, increase the likelihood of continued
land-cover changes, forest loss and degradation (Estrada, 2013; Estrada et
al., 2017). Documenting the ability of primates to use the matrix between
fragments and identifying agricultural land-use practices compatible with
primate survival, reproduction and/or dispersal across the landscape is
imperative for developing guidelines for landscape management that reconcile
primate conservation with subsistence of local communities (Estrada, 2013;
Flesher, 2015).
Golden-headed lion tamarins (Leontopithecus chrysomelas) are frugivorous group-living primates of the
Atlantic Forest of south Bahia (Brazil) that are classified as endangered and under
threat from habitat loss, fragmentation and degradation (Kierulff et al.,
2008). The landscape in south Bahia (Brazil) is a mosaic of Atlantic Forest
remnants embedded within an agricultural matrix dominated by shaded cacao
(Theobroma cacao) agroforests, locally known as cabruca (shaded cacao plantations in which the
middle and understory trees of intact forests are removed and replaced with
cacao trees; Alger and Caldas, 1994). Other economically important crops are
present within the matrix, namely bananas (Musa paradisiaca)
and rubber (Hevea brasiliensis), in addition to
lesser quantities of coconut palm trees (Cocos nucifera) and manioc (Manihot esculenta) (IBGE, 2014).
Golden-headed lion tamarin home ranges can encompass mature and degraded
forests, in addition to cabruca (Raboy and Dietz, 2004). To date, no studies have
reported the species using any other type of vegetation within the matrix,
although the use of non-monoculture rubber plantations is suspected by
former researchers in the area (B. E. Raboy, personal communication, 2014). Given that the
long-term survival of this species may depend on its ability to use the
matrix between fragments across its geographic range, this study aimed to
investigate this potential use of rubber plantations.
We report on the presence of a group of golden-headed lion tamarins in a
rubber plantation on a farm in south Bahia, thus constituting the first
systematic observation of the species using this form of land use within the
matrix; and we provide preliminary information on the group's behaviour and use
of space in a fragmented landscape dominated by agricultural land use.
Methods
The fieldwork was conducted on a 29.4 ha privately owned farm, Fazenda Santo
Antônio (-15.283796∘; -39.134477∘) in the
municipality of Una (Bahia), in south Bahia. Approximately 35 % of the
farm comprises patchy evergreen forest, while the remaining 65 % is
planted with perennial rubber, cupuaçu (Theobroma grandiflorum),
soursop (Annona muricata), pepper (Piper nigrum),
bananas and ephemeral crops such as manioc and garden vegetables.
The farm also
includes a 30-year-old rubber plantation of approximately 2.5 ha surrounded
by secondary forest patches, agricultural plantations and open fields. Many
of the older rubber trees bear epiphytic bromeliads of various sizes.
Additional trees, such as cacao, banana, jackfruit (Artocarpus heterophyllus) and guava (Psidium guajava), are
interspersed with the rubber trees (Fig. 1).
Data on total time spent with the focal group, use of natural
vegetation types and rubber plantation, occurrence of associations with
Wied's marmosets, use of sleeping sites and other behaviours
observed over 22 observation days between August 2013 and January 2014.
DateTotal time with group (h:min)Vegetation types used1Seen in rubber plantation?Seen in association?Identity2 and location of sleeping tree Behaviours observed while in rubber plantationMorningEveningLocation12/08/20131:45–YesYes–OJR01Rubber plantationIntraspecific and interspecific grooming, sleeping19/08/20130:03–YesNo–OJR01.Rubber plantationSleeping22/08/20132:30MSNoYes–––23/08/20133:19MSNoYes–––2/10/20133:05MSYesNo–OJR01Rubber plantationEating jackfruit, travelling, sleeping3/10/20136:29MS.YesYesOJR01–Rubber plantationTravelling, hiding, sleeping22/10/20130:59–YesYesOJR01–Rubber plantationTravelling, sleeping(together with marmosets)23/10/20135:18AS, ISNoNo–––24/10/20134:03AS, ISYesYesOJR01–Rubber plantationEating jackfruit, travelling, sleeping29/10/20136:30–YesYesOJR01–Rubber plantationTravelling, sleeping4/11/20132:07MSNoNo–––5/11/20135:41–YesYesOJR01–Rubber plantationTravelling, sleeping6/11/20135:20ASNoNoOJR02–AS–13/11/20136:07ASYesNoOJR01–Rubber plantationTravelling, sleeping14/11/20135:29–YesYesOJR01–Rubber plantationEating jackfruit, travelling, sleeping15/11/20133:54–YesYesOJR01–Rubber plantationEating jackfruit, travelling, grooming, sleeping20/11/20130:48–YesYesOJR01–Rubber plantationEating jackfruit, travelling, sleeping4/12/20131:28RFYesNoOJR01–Rubber plantationEating jackfruit, travelling, sleeping6/01/20141:00RFYesNoOJR01–Rubber plantationTravelling, sleeping14/01/20140:26–YesYesOJR01–Rubber plantationTravelling, sleeping, scentmarking21/01/20141:35MS, ASNoNo–––24/01/20141:21–YesNoOJR01–Rubber plantationTravelling, sleeping
1 Abbreviations used: AS, advanced stage secondary vegetation;
MS,
medium stage secondary vegetation; IS, initial stage secondary vegetation;
RF, regenerating field.2 Individual trees received unique codes composed of
letters and a unique number.
Maps of the study area, based on the interpretation of a georeferenced aerial photo obtained from Google Earth (image date:
27 May 2010). The upper map shows the property borders and locations where a group of golden-headed lion tamarins
was sighted between August 2013 and January 2014. The map below provides information on the different natural
vegetation types and forms of land use in different areas of the property, and the locations where the group was seen in association with Wied's marmosets.
The black marker in the smallest frame indicates the location of the study area in Brazil.
Data collection
Following approval by the Brazilian authorities (Permit no. SISBIO N
23457-3), we employed a trained field assistant to start searching daily for
groups of golden-headed lion tamarins on the farm. We recorded their
behaviour using the following categories: travelling, remaining stationary,
foraging for fruit, eating fruit, foraging for flowers, eating flowers, foraging for
animals, eating animals, socialising, resting and “other”, as described
in the ethogram in Raboy and Dietz (2004). From August 2013 through January
2014, we conducted ad libitum observations to identify groups of
golden-headed lion tamarins. To facilitate habituation and monitoring, we
captured a group of three golden-headed lion tamarins on 28 September 2013
in a degraded forest patch adjacent to the rubber plantation, using
platforms armed with Tomahawk live traps (trap measures: 48.3 cm × 15.2 cm ×
15.2 cm) and baited with bananas (following procedures described in Dietz et
al., 1996). In the field laboratory, the animals were identified as two
males and one female weighing 614, 617 and 637 g respectively,
indicating adult ages (adult weight range: 500–800 g; Oliveira et al., 2011).
One male and the female were fitted with a radio collar (Holohil, RI-2D) to
facilitate ongoing habituation and monitoring. All procedures complied with
legal requirements from Brazil and applicable international and
institutional guidelines for the care and use of animals.
Subsequently, we started the habituation process. We located the group on
1–4 days/week at their sleeping site in the morning using radio-telemetry.
We followed the group for as long as possible during the day until it
retired to a sleeping site for the night. We terminated observations if we
had the impression that our presence was causing the group to hide and might
have prevented them from foraging sufficiently before locating a suitable
sleeping tree for the night (see Table 1).
We recorded the following information at 20 min intervals: GPS location of
the group (using a handheld GPS 92Xs unit); habitat type (rubber plantation);
advanced, medium or initial secondary forest; open or regenerating fields
(for definitions see Catenacci et al., 2009); and agricultural areas; in
addition to ad libitum observations on behaviour. We did not calculate the
total time the group spent in each vegetation type because of a possible
bias as a result of the process of habituation.
Group locations were subsequently entered into ArcGIS 10.4.2 and plotted on
a georeferenced image of the study area downloaded from Google Earth Pro
(image date: 27 May 2010). We further added layers with additional
information on the location of property borders as obtained from the
owner's legal registration documents, and the location of
different natural vegetation types and agricultural areas as identified on
the ground.
Results
Between August 2013 and January 2014, we spent 103.5 h in the field, 69.28 h
of which were in the presence of the group (meaning we either had visual contact
or were within a few metres of the spot where we knew them to be hiding). We
saw the group in the rubber plantation on 16 of 22 observation days (73 %)
during which we were able to establish visual contact (Table 1; Fig. 2).
Additional vegetation types used were initial, medium and advanced secondary
forest, and a regenerating field.
On 17 occasions (77 % of observation days), we were able to determine the
group's sleeping site in the morning or evening. In 16 of these 17 occasions
(94 %), the group used one particular individual palm tree locally known
as “catulé” (Syagrus sp., Family Arecaceae) at the
northern edge of the rubber plantation, bordering a passion fruit plantation
(Table 1; Fig. 2).
We saw Wied's marmosets (Callithrix kuhlii) together with the group in the rubber
plantation on 10 of 16 sightings (63 %), occurring either in the rubber
plantation or in the small patch of degraded forest located to the north of
the rubber plantation (Table 1; Fig. 2). We observed the group of
golden-headed lion tamarins using both this northern edge of the rubber
plantation, where the palm tree sleeping site is located, and the area along
a central line running north to south through the rubber plantation. We also
observed the group in a patch of advanced secondary forest to the southeast
of the rubber plantation encountering another group of golden-headed lion
tamarins just across the border on the neighbouring property. We recorded
the group eating in a jackfruit tree in the centre of the plantation. We
additionally observed allogrooming, feeding and scent-marking behaviour
during waking hours in the rubber plantation, in addition to hiding and
travelling.
Discussion
This study is the first to provide evidence of the use of a rubber
plantation in south Bahia by golden-headed lion tamarins. We observed rubber
plantation use on the majority of study days. On several occasions, we saw
the group in association with Wied's marmosets and observed
behaviours such as eating, sleeping and grooming, thus suggesting that the
group may have been using the plantation as part of its home range and not
merely as a corridor between fragments. We further observed selective site
use, in the sense that the group used some areas of the rubber plantation
more than others; however, given the preliminary nature of our observations
and the limited number of observation days (due to being early in the
habituation process), further investigation is needed to confirm this
pattern. We are currently following this and two more groups to study how
they use rubber plantations spatially (entire area vs. edges; specific
pathways) and to obtain detailed information on their resource use and
behaviour.
Golden-headed lion tamarins have long been thought to depend on mature
forests for survival, due to their requirement of resources such as epiphytic
bromeliads for foraging and tree holes for sleeping (Rylands, 1996). More
recent studies have reported the species being able to survive and reproduce in
secondary forests, including cabruca agroforests (Catenacci et al., 2016; Oliveira
et al., 2011). Being predominantly a frugivore, the species' diet varies
between areas, reflecting differences in floristic composition and plant
density; this indicates that the species adapts easily to changes in fruit
availability (Catenacci et al., 2016). The extent to which the availability
of sufficient sleeping sites and/or foraging sites limits its capacity for
exploring altered habitats is as of yet undocumented. Therefore, maintaining a
forest mosaic that includes patches of forest providing these resources is
considered important (Catenacci et al., 2016). The rubber plantation in this
study is relatively old (approx. 30 years) and infrequently managed through
annual removal of undergrowth. With respect to potential resources for
golden-headed lion tamarins, several of the older rubber trees bear
epiphytic bromeliads, providing potential microhabitats for insect foraging
(Raboy and Dietz, 2004). Bromeliads are listed as principal foraging sites
at all study areas where golden-headed lion tamarins have been observed
(Raboy and Dietz, 2004; Guidorizzi, 2008; Oliveira et al., 2011; Catenacci
et al., 2016). Although we did not record our study group foraging in
bromeliads in the rubber plantation during the observation period described
here, we observed this behaviour at a later time. We suspect the lack of
bromeliad foraging during the study period to be due to the habituation
process, which frequently caused the group to hide, usually in bromeliads,
and made the visualisation of feeding and foraging behaviour more difficult.
In addition to bromeliads, the rubber plantation contains some native fruit
trees from plants included in the species' diet (e.g. Tapirira guianensis; Oliveira et al.,
2010) and jackfruit trees. Jackfruit, an exotic species introduced in
Brazil in the 18th century, is widely distributed along the Brazilian coast
(Correia, 1975). Many animal species consume its fruits, including
Leontopithecus chrysomelas; the consumption of jackfruit has been observed at all sites in
the ombrophyllous forest where this primate has been studied (Raboy and Dietz,
2004; Oliveira et al., 2011; Catenacci et al., 2016).
All of these resources may attract golden-headed lion tamarins to these
plantations and could therefore be used as a parameter to evaluate the
suitability of rubber plantations for use by golden-headed lion tamarins and
possibly Wied's marmosets. We advocate further investigation
of this hypothesis, since the gained knowledge may help in defining
management practices that aim at increasing the suitability of rubber
plantations for both species.
Implications for conservation
Rubber agroforest systems in Asia can support local biodiversity and
constitute an important component of sustainable land use, reconciling
conservation with local community subsistence and development (Warren-Thomas
et al., 2015). The present study demonstrates that such systems may also be
used by golden-headed lion tamarins in the fragmented forests of
south Bahia. Cacao is the main economic product of Bahia, particularly so in
the municipalities within the species' distribution range
(with 547 722 ha destined for production), followed by bananas. However,
rubber constitutes the third-ranking crop in terms of area reserved for
harvesting (IBGE, 2014), with 33 521 ha of land destined for rubber
production in Bahia, approximately one third of which is located within the
distribution range of the golden-headed lion tamarin (IBGE, 2014). In
economic terms, rubber offers the additional benefit of guaranteeing a
steady monthly income for farmers, since the trees provide a daily
harvestable flow of latex in contrast to cacao which is harvested
seasonally, thus providing an income during only a few months of the year
(Schroth and Ruf, 2014). Rubber can be an important additional crop,
particularly for farms too small to produce enough cacao to generate income
for an entire year. In addition to shaded cacao plantations, rubber
plantations with a structure that facilitates use by groups of golden-headed
lion tamarins, either as a corridor or an extension of their home range, may
constitute a land-use type that ensures functional connectivity between
forest fragments for golden-headed lion tamarins, reconciling local
development and conservation while adding value to rubber production and
increasing the available habitat for these endangered primates.
The data set on which this article was based on is available at
10.13140/RG.2.2.15797.68328 (De Vleeschouwer and Oliveira, 2017).
The authors declare that they have no conflict of interest.
Acknowledgements
We thank our assistant Josinei da Silva Santos and the family Ribeiro dos
Santos for permission to work on their property. Funding was provided by the
Centre for Research and Conservation of the Royal Zoological Society of
Antwerp. The Flemish Ministry of Economy, Science and Innovation provided
structural funding to the Centre for Research and Conservation. We thank
Nikki Tagg for the comments on the manuscript and language editing, and we thank two
anonymous reviewers for their helpful comments on an earlier version of this
manuscript.
Edited by: D. Zinner
Reviewed by: two anonymous referees
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