The importance of orangutans in small fragments for maintaining metapopulation dynamics

Abstract

Orangutans (Pongo spp.) occur at low densities and therefore large areas are necessary to sustain viable metapopulations, defined here as sets of conspecific units of individuals linked by dispersal. Historically, orangutans lived in large contiguous areas of intact rainforest, but are now increasingly found in agricultural and other landscapes modified by people. Here we collate evidence of orangutans utilizing isolated forest fragments (< 500 ha) within multiple-use landscapes dominated by oil palm monoculture across Borneo. Orangutan signs (i.e. nests) were evident in 76 fragments surveyed by helicopter, and in 50 of 70 additional fragments surveyed on the ground; on average 63 ha in size. This includes presence of adult resident females with dependent young confirmed in 40% of the fragments assessed by ground survey. Our study revealed some resident females are raising offspring in isolated forest patches within mature oil palm stands. This not only confirms that some forest patches can sustain orangutans, but indicates migratory males are capable of reaching these fragments scattered throughout the multiple-use landscape. Therefore, orangutans that use or live in even small isolated forest patches are an essential part of the overall metapopulation by maintaining gene flow between, and genetic connectivity within, populations distributed across larger multiple-use landscapes. Orangutan survival is commonly thought to be low in small, isolated forest patches, and the customary management strategy is to remove (translocate) these individuals and release them in larger forests. In some cases, translocations may be necessary, i.e. in case of fire or when the animals are in eminent danger of being killed and have no other refuge. However, the small amount of data available indicates that mortality rates during and after translocations are high, while the impacts of removing animals from spatially dispersed metapopulations are unknown. Therefore, we argue the current policy of routine translocation rather than conserving the species within human-modified landscapes could inadvertently decrease critical metapopulation functionality necessary for long-term viability. It is clear that orangutans need natural forest to survive, but our findings show that fragmented agricultural landscapes can also serve as complementary conservation areas in addition to fully protected areas if they are well designed with ecological connections, and if orangutan killing can be prevented. To achieve this, we call for a paradigm shift from the traditional large single forest model to one that emphasizes metapopulation functionality in the fragmented forest - human use matrix characteristic of the Anthropocene.

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The importance of orangutans in small fragments for maintaining
metapopulation dynamics
Marc Ancrenaz1,2,3*, Felicity Oram3, Nardiyono4, Muhammad Silmi5, Marcie E. M. Jopony6,
Maria Voigt7,8, Dave J.I. Seaman7, Julie Sherman9, Isabelle Lackman1, Carl Traeholt10, Serge
Wich11,12, Matthew J. Struebig7, Truly Santika7,13,14, Erik Meijaard2,7,13
1HUTAN, Sandakan, Sabah, Malaysia
2Borneo Futures, Brunei Darussalam
3Pongo Alliance, Kuala Lumpur, Malaysia
4PT Austindo Nusantara Jaya Tbk., Jakarta 12950, Indonesia
5United Plantations berhad / PT Surya Sawit Sejati, Kalimantan Tengah, Indonesia
6Wilmar International Ltd, Singapore
7Durrell Institute of Conservation and Ecology, University of Kent, Canterbury, UK
8German Centre for Integrative Biodiversity Research (iDiv) Halle – Jena – Leipzig, Deutscher Platz
5e, 04103 Leipzig, Germany
9Wildlife Impact, Portland, Oregon, USA
10Copenhagen Zoo, Denmark
11School of Biological and Environmental Sciences, Liverpool John Moores University, Liverpool,
UK
12Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, Amsterdam, The
Netherlands
13School of Biological Sciences, University of Queensland, St Lucia, Australia
14Natural Resources Institute (NRI), University of Greenwich, Chatham Maritime, ME4 4TB, UK
* Correspondence:
Marc Ancrenaz
marc.ancrenaz@gmail.com
Keywords: Borneo, conservation, ecology, Indonesia, Malaysia, oil palm, Pongo pygmaeus,
translocation
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Abstract
Orangutans (Pongo spp.) occur at low densities and therefore large areas are necessary to sustain viable
metapopulations, defined here as sets of conspecific units of individuals linked by dispersal. Historically,
orangutans lived in large contiguous areas of intact rainforest, but are now increasingly found in agricultural
and other landscapes modified by people. Here we collate evidence of orangutans utilizing isolated forest
fragments (< 500 ha) within multiple-use landscapes dominated by oil palm monoculture across Borneo.
Orangutan signs (i.e. nests) were evident in 76 fragments surveyed by helicopter, and in 50 of 70 additional
fragments surveyed on the ground; on average 63 ha in size. This includes presence of adult resident females
with dependent young confirmed in 40% of the fragments assessed by ground survey. Our study revealed
some resident females are raising offspring in isolated forest patches within mature oil palm stands. This not
only confirms that some forest patches can sustain orangutans, but indicates migratory males are capable of
reaching these fragments scattered throughout the multiple-use landscape. Therefore, orangutans that use or
live in even small isolated forest patches are an essential part of the overall metapopulation by maintaining
gene flow between, and genetic connectivity within, populations distributed across larger multiple-use
landscapes. Orangutan survival is commonly thought to be low in small, isolated forest patches, and the
customary management strategy is to remove (translocate) these individuals and release them in larger forests.
In some cases, translocations may be necessary, i.e. in case of fire or when the animals are in eminent danger
of being killed and have no other refuge. However, the small amount of data available indicates that mortality
rates during and after translocations are high, while the impacts of removing animals from spatially dispersed
metapopulations are unknown. Therefore, we argue the current policy of routine translocation rather than
conserving the species within human-modified landscapes could inadvertently decrease critical
metapopulation functionality necessary for long-term viability. It is clear that orangutans need natural forest to
survive, but our findings show that fragmented agricultural landscapes can also serve as complementary
conservation areas in addition to fully protected areas if they are well designed with ecological connections,
and if orangutan killing can be prevented. To achieve this, we call for a paradigm shift from the traditional
large single forest model to one that emphasizes metapopulation functionality in the fragmented
forest – human use matrix characteristic of the Anthropocene.
1 Introduction
In international wildlife conservation, the prevailing policies and conservation strategies in
governmental and non-governmental organizations have favored large, connected “natural” areas,
especially in tropical conservation, such as the “Heart of Borneo”, or the “Central Forest Spine” of
West Malaysia. These strategies often consider fragments of natural habitat as of little or no value for
wildlife conservation (Sodhi et al., 2010). However, the importance of small habitat patches for
biodiversity conservation is increasingly recognized (Edwards et al., 2019; Wintle et al., 2019),
especially for wide-ranging species such as large mammals or volant species (Beca et al., 2017; Melo
et al., 2017).
Prior to the arrival of modern humans in Asia, orangutans presumably depended on primary forest for
survival, but researchers have recently documented their resilience to drastic habitat changes (Spehar
et al., 2018). Orangutans persist and reproduce in forests logged for timber (Husson et al., 2009;
Ancrenaz et al., 2010), in industrial timber plantations (Meijaard et al., 2010; Spehar and Rayadin,
2017) and in agricultural landscapes, for example (Campbell-Smith et al., 2011). They are also found
in isolated patches of forest within landscapes that have been extensively transformed by humans,
albeit at lower densities than in more extensive natural forests (Ancrenaz and Lackman, 2014;
Ancrenaz et al., 2015; Spehar et al., 2018; Seaman et al., 2019). Orangutan survival and population
viability within these heavily managed landscapes is likely contingent on hunting and killing being
minimized (Marshall et al., 2006; Husson et al., 2009).
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Although orangutans are solitary foragers, they live in an abstract community of known and related
individuals, where females are resident and males disperse (Arora et al., 2012). Female orangutans
are philopatric and strongly tied to their natal area, and the home ranges of maternal kin often overlap
considerably (van Noordwijk et al., 2012). They display extreme long-term site fidelity with the core
of their home range and are reluctant to move under normal circumstances (Ashbury et al., 2020).
Adult flanged males will aggressively defend an area with females in it, especially when females are
sexually active (Spillmann et al., 2016).
Currently, orangutans found in small forest patches are generally perceived as “non-viable”, because
of insufficient food, the risk of getting killed by people, or because of fires and logging threatening
remaining trees (Sherman et al., 2020). Consequently, many wild orangutans observed in such habitat
patches are pre-emptively translocated to nearby forests presumed more suitable for their survival.
For example, in Indonesian Borneo between 621 and 1,124 wild orangutans were “rescued” from
forest fragments in human-modified landscapes between 2007 and 2017 and translocated to other
forest areas (Sherman et al., 2020). Very little is known about the survival rate of individuals
following translocation, but rare post-translocation monitoring indicates that translocated orangutans
struggle to survive (Sherman et al., 2020). In addition, females released into new forest areas will
likely not move far from the point of release (Lokuciejewski, 2018). In areas with existing resident
females, competition for food increases, potentially displacing newly arrived females from the
release site - or vice versa (Marzec et al., 2016).
The impacts on orangutan metapopulation of removing individuals from forest patches are poorly
understood, but could intensify the effects of fragmentation and jeopardize long-term viability.
Information on the counterfactual – i.e. what would have happened to orangutans had they not been
removed from patches – would be useful. In the Kinabatangan area of Malaysian Borneo, for
example, orangutans have been recorded regularly for >20 years in most small forest patches
available in the oil palm dominated landscape (Ancrenaz et al., 2015, and HUTAN, unpubl. data).
Some animals travel through the farmland between forest patches, and some resident females
reproduce successfully (Ancrenaz et al., 2015; Spehar et al., 2018). Rather than being completely
isolated, these individuals form a larger metapopulation, where conspecific groups of individuals are
linked by dispersal (Hastings and Harrison, 1994). The combination of multiple orangutan groups
living in forest patches irrespective of their size or protection status is inherently important to the
long-term conservation of the species (Voigt et al., 2018).
Here, we build on the experience from the Kinabatangan area and compile evidence of orangutans
utilizing forest patches in other human-modified landscapes of Borneo. We refine current
understanding and knowledge gaps about the persistence of the species fragmented landscapes, and
provide recommendations for conservation management.
2 Evidence of orangutans utilizing forest patches
2.1 Aerial surveys
Aerial surveys were conducted in 2008, 2012, and 2018 to assess orangutan presence in forest
patches across the agricultural landscapes of Kinabatangan, South Sandakan Bay, Segama, Beluran
and Sugut. Surveys were conducted from a Bell 206 helicopter at about 60 knots and ca. 100 m above
the canopy, following protocols established in Sabah (Ancrenaz et al. (2005). Patches were
categorized based on their size (very small: < 5 trees; small: 5 trees to <1 ha; medium: 1-10 ha; large:
>10 ha), and orangutan nests and signs of human disturbance recorded (see Ancrenaz, 2015). We
limited our aerial investigation to patches <500 ha, which corresponds to the upper limit of a female
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range in most areas (Singleton et al., 2009). A forest fragment was considered isolated if the closest
forest was >500 m away.
The 2008 surveys revealed >500 orangutan nests in 76 small forest patches, <100 ha (including a
“patch” with one single tree) that were completely isolated within mature oil palm plantations:
Kinabatangan (32 patches; >100 nests); Sandakan Bay (eight patches; >100 nests); Sugut (15
patches; > 150 nests); Beluran (seven patches; >50 nests); Lower Segama (14 patches; >100 nests).
The same route over Kinabatangan in 2012 confirmed 15 of the 32 patches were still present (i.e.
53% of the patches had been cleared) and detected >120 nests in 12 of them (Ancrenaz et al., 2015).
In 2018, the repeated survey of Sugut recorded significant deforestation, though all of the seven
patches of degraded forest surveyed contained nests (> 60 in total).
2.2 Ground and interview surveys
In 2019 and 2020, rapid ground surveys revealed orangutans utilizing forest patches in 11 oil palm
estates in Sabah and Kalimantan. Nests were often built on taller trees that offered vantage points,
although several were detected in oil palms close to forest. We interviewed plantation workers and
managers at these sites about orangutan presence and potential conflicts in their estates, using a
previously tested protocol (Meijaard et al., 2011; Ancrenaz et al., 2015). Respondents revealed that in
seven estates (four in Sabah, three in Kalimantan) they recognized mothers with their young in and
around the same patches (12 occupied by nine females). Two respondents stated the same females
(four in total) were regularly observed over 5-10 years. Flanged males and smaller individuals
(usually without an infant, which could indicate an unflanged or a young male) were reported
walking on the ground in oil palm between forest patches. Crop conflicts were rare, and mostly
occurred on young palms <3 years old. Most damage to mature palms occurs within the first two
rows of palms located along borders with areas of natural forest. Although it was reported that some
damages could impair flower and fruit productivity, estate managers interviewed did not consider
damage to mature palms (i.e. above 5 years old) a concern.
To complement the results of our rapid ground surveys in February 2020 we sent a questionnaire to
four of the oil palm estates, and to three orangutan researchers working in fragmented forest
landscapes. Respondents were asked to categorize forest patches in their landscapes by location and
size; as a natural forest corridor(s) to larger forest areas; presence or absence of orangutans, including
direct sightings of the individuals and indirect sightings, such as nests or pictures from camera traps.
The survey covered nine oil palm landscapes, comprising 81 patches; 11 of those were larger than
our size threshold (>500 ha) and are not reported here (although they all supported orangutans).
Camera traps or direct sightings confirmed orangutans in 50 of 70 patches (i.e. 71% of the total) with
an average patch size of 57 ha (range: 1-286 ha; SD=72 ha). Signs were detected in 14 of 19 patches
<10 ha in size; 18 of 26 patches of 10-50 ha; 9 of 10 of 50-100 ha, and 9 of 15 of 100-500 ha (Figure
1).
Seventy two percent of patches with orangutan signs were >500 m from the nearest forest and
considered “isolated”. Presence of an adult female with young was confirmed in 21 fragments (10-
236 ha in size; mean 71; SD= 69), and 12 were completely isolated. In 10 additional patches signs of
adult females without young, or unflanged males (these two classes being very difficult to
distinguish), were reported. Flanged males were present in four patches, and 15 patches had signs of
orangutan nests without any indication of age and sex. Orangutans were absent from 20 patches at
the time of surveys (0.5-369 ha in size; mean 81 ha; SD 101 ha), 13 of which were isolated (Figure
1).
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Orangutans regularly use forested corridors set aside by estates between forest patches, such as
riparian buffers along rivers, or “pathways” designated to enhance connectivity across the landscape.
For example, to link two isolated forest patches one estate created a 40 m wide corridor 1.2 km long,
comprising trees that had been planted under palms. Orangutan nests were observed in this corridor
within four years, confirming use for dispersal. During our site visits, the three large corridors
between forests that we assessed had nests, illustrating that corridors are important for resting
(nesting) and for dispersing across the landscape.
3 Discussion
Our collation of reports from agricultural landscapes demonstrates substantial use of forest fragments
by orangutans in farmland. It is increasingly evident that orangutans are a highly flexible and
adaptable species that can maintain high population densities in production forests (Ancrenaz et al.,
2010; Oram, 2018; Roth et al., 2020), and most wild orangutan populations in Borneo are currently
found outside of strictly-protected forests (Santika et al., 2017; Voigt et al., 2018). Orangutans in
these landscapes can cope with degradation in habitat structure such as canopy opening (Davies et al.,
2017), disperse on the ground when necessary (Ancrenaz et al., 2014), reproduce, and even
successfully raise young to maturity (van Noordwijk et al., 2018).
In extensive oil palm plantations, orangutan presence is more prevalent close to forest edges or
within patches inhabited by resident individuals, as already documented in Kinabatangan (Ancrenaz
et al., 2015). However, both flanged and unflanged males have been recorded to venture several km
inside plantations (Ancrenaz et al., 2015). Female orangutans are reluctant to leave their natal area in
Bornean forest (Arora et al., 2012; van Noordwijk et al., 2012), and this may also be the case in forest patches:
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some are not only surviving, but raise offspring in isolated patches many years after planting oil palm.
These individuals probably survived the initial phase of forest loss when oil palm estates were
established and took refuge in small forest patches retained within the modified landscape. Over the
years, they maintained their ranging patterns by visiting and using as many forest patches within their
former home-range as possible, even if most of this home-range is currently covered with palms or
other agricultural crops (Figure 2). Of course, sufficient food resources are needed for these females
to survive and reproduce in these fragmented landscapes. Their chances of long-term survival are
likely increased with the number, size and quality of forest fragments. In some places, enrichment
planting of key food species, and improving the overall forest connectivity within the agricultural
landscape will also be important for increasing survival.
Figure 2. Schematic representation of the metapopulation functioning of orangutans in fragmented
landscapes.
The presence of offspring in these isolated patches suggests migrating males are likely using the
human-modified landscape to search for receptive females. Indeed, males are the most frequently
observed sex in oil palm plantations generally, including numerous mentions of them walking on the
ground, along rivers or streams and even on plantation roads. During these travels, orangutans may
use any vantage point (such as isolated trees) to navigate within the plantation as suggested by the
frequent report of nests built in scattered single trees, or small groups of trees, within plantations far
away from any forest. Orangutans also appear to use forest corridors to move across the landscape, as
recorded by Seaman et al. (2019) and our surveys in commercially administrated lands. These
corridors are often set aside as high conservation value forests to meet sustainability certification
criteria, either as riparian buffers or other linkages between forest patches.
Further investigation is warranted before we can consider a primarily agricultural landscape as viable
long-term habitat for orangutans. Many questions still need to be addressed, for example: Are
orangutan dietary needs met in plantation settings?; What is the fate of young individuals that grow
up in small isolated fragments?; How can we get local people and companies to agree living
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alongside orangutans?; or What are the risks associated with the persistence of fragments as viable
habitats (e.g. edge effects, fire, inbreeding, intrusion, etc.) and edge effects? Many questions remain,
but it is clear that we need to revisit our thinking about what encompasses a viable orangutan
population. The traditional way of thinking of populations as a group of orangutans in a contiguous
forest would ultimately result in a disjunct distribution range with isolated populations no longer
connected genetically. Long-term maintenance of habitat stepping-stones within larger
multifunctional landscapes, on the other hand, could retain connectivity between the larger forest
areas and boost the overall chances of survival for the population as a whole. Therefore, conservation
efforts for orangutans, and other endangered tropical species, must begin to recognize the critical role
habitat fragments may play to help stabilize landscapes for orangutans at the metapopulation level.
Government and non-government organizations need to join forces and acknowledge that orangutan
survival is best guaranteed through overall management of metapopulations.
Recognizing that orangutan viability hinges on metapopulation integrity also requires a change in
perceptions about “rescuing” and translocating individuals. While there are obvious threats to
orangutans living in forest fragments (physical harm, killing, or forest destruction), a recent analysis
of wild-to-wild translocation in Kalimantan showed that at least 90% of the individuals captured
were healthy and several of them had healthy infants as well (Sherman et al., 2020). These animals
had managed to survive in habitats perceived as inhospitable by orangutan conservation practitioners.
Therefore, we argue that, rather than emptying small forest patches of orangutans as a default
operational practice, local authorities and conservation organizations must develop more proactive
solutions, where forest patch management fosters measures to allow people and orangutans to co-
exist safely. We also argue that removing individuals (especially resident females) could be
deleterious to the overall metapopulation functioning of fragmented populations; it may threaten both
the orangutan metapopulation functionality at the translocation site, as well as be potentially
catastrophic not only to the individual, but the metapopulation at the release site as well. There are at
least 10,000 orangutans in multiple use landscapes (Meijaard et al., 2017) and rescuing all is
unfeasible, thus requiring in situ management given its protected status. It also recognizes that is
neither non-zero during wild-to-wild translocations (Wilson and McMahon, 2006), nor following
reintroduction (Galdikas, 2018; Sherman et al., 2020).
An additional key problem with translocations is that once the orangutans are removed from a forest patch (or
at least those animals that could be captured), the forest patch and its other remaining wildlife are more likely
to be converted to human use, because the forest patch has lost what little protection it received from
containing orangutans as a legally protected species. Indeed, the presence of a fully protected species in a
forest fragment confers to this fragment a status of “High Conservation Value” with a specific set of
management measures, including no-deforestation requirements, and this reduces the likelihood of conversion
(Carlson et al., 2018). If not protected, the loss of the forest patch would then also mean the loss of all other
wildlife that was not rescued as well as loss of ecosystem services provided by the forest (Lucey et al., 2014;
Wells et al., 2016).
Of course, there remain circumstances when the health of animals surviving in small fragments is
compromised (e.g. food scarcity, habitat destruction (K. Sanchez, pers. com.), and in such cases,
translocations will still be needed when the alternative is a dead orangutan. Our paper is not against
translocation as a part of the overall conservation toolbox, but we emphasize that this kind of
intervention should be the exception rather than the norm. Governments tend to support
translocations as it provides a means for them to allow developments to go ahead in unprotected
forest areas (Meijaard, 2017), and it is important that the conservation community respects the legal
principle that orangutans are protected species, whether they occur inside or outside protected areas.
Ongoing discussion with government authorities is needed to ensure that the focus of orangutan
conservation strongly remains on in situ protection of remaining populations.
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4 Conclusion
Insights from our current studies require that we reassess the notion of orangutan population viability
in human-modified landscapes. Orangutan populations in a contiguous forest area containing fewer
than 50 individuals are generally thought to be non-viable (Utami-Atmoko et al., 2019), and as a
result are often relocated. However, such a policy overlooks the fact that (1) this is a species that
exists at low densities even in ideal conditions, and therefore functions as a metapopulation or set of
conspecific groups of individuals linked by dispersal across wide distances; and (2) that in today’s reality
on Borneo and Sumatra many forest fragments are not large enough to contain more than 50 animals. The
good news, as we demonstrate here, is that metapopulations are still functioning in mixed-use
landscapes so gene flow is still possible. In other words, most populations across fragmented
landscapes could be viable if we manage to maintain essential habitat fragments and prevent any
unnatural deaths or removal from the landscape. Therefore, the conservation unit to be managed
should then not be the animals in relatively well-protected larger forest areas, but the metapopulation
that is ranging across the entire mixed protected–privately administered landscape as a whole.
Eventually, the future of orangutans in the Anthropocene will primarily depend on the attitude of all
land users and government that should target a peaceful coexistence between people and orangutans
outside and inside protected areas.
Acknowledgments
In addition to all HUTAN supporters we thank the United States Fish and Wildlife Service Great Ape
Conservation Fund for financial support [grant number F17AP01081], the Arcus Foundation, New
York, NY [grant number G‐PGM‐1610‐1985], the IUCN Species Survival Commission Primate
Specialist Group - Section on Great Apes [project grant number P02472], the Yayasan Sime Darby
and the French Alliance for Preservation of Forests. The funders had no involvement in study design,
in the collection, analysis and interpretation of data, or in the writing of the paper and the decision to
submit the article for publication.
Author contributions
MA, FO, IL and EM initially conceptualized this study. FO, NA, DS, MJ, MS, Simli, and CT
contributed data. MV helped with data analysis and diagram design. MA, EM, FO, JS, CT, MS, MV,
and DS helped improve the manuscript.
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial
relationships that could be construed as a potential conflict of interest.
Data Availability Statement
The datasets analyzed for this study can be found in the XXXX.
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