Assessing the impact of forest structure disturbances on the arboreal movement and energetics of orangutans—An agent-based modeling approach

This is the final version. Available from Frontiers Media via the DOI in this record. Data availability statement: The datasets presented in this study can be found in online repositories. The names of the repository/repositories and accession number(s) can be found in the article/Supplementary material.Agent-based models have been developed and widely employed to assess the impact of disturbances or conservation management on animal habitat use, population development, and viability. However, the direct impacts of canopy disturbance on the arboreal movement of individual primates have been less studied. Such impacts could shed light on the cascading effects of disturbances on animal health and fitness. Orangutans are an arboreal primate that commonly encounters habitat quality deterioration due to land-use changes and related disturbances such as forest fires. Forest disturbance may, therefore, create a complex stress scenario threatening orangutan populations. Due to forest disturbances, orangutans may adapt to employ more terrestrial, as opposed to arboreal, movements potentially prolonging the search for fruiting and nesting trees. In turn, this may lead to changes in daily activity patterns (i.e., time spent traveling, feeding, and resting) and available energy budget, potentially decreasing the orangutan's fitness. We developed the agent-based simulation model BORNEO (arBOReal aNimal movEment mOdel), which explicitly describes both orangutans' arboreal and terrestrial movement in a forest habitat, depending on distances between trees and canopy structures. Orangutans in the model perform activities with a motivation to balance energy intake and expenditure through locomotion. We tested the model using forest inventory data obtained in Sebangau National Park, Central Kalimantan, Indonesia. This allowed us to construct virtual forests with real characteristics including tree connectivity, thus creating the potential to expand the environmental settings for simulation experiments. In order to parameterize the energy related processes of the orangutans described in the model, we applied a computationally intensive evolutionary algorithm and evaluated the simulation results against observed behavioral patterns of orangutans. Both the simulated variability and proportion of activity budgets including feeding, resting, and traveling time for female and male orangutans confirmed the suitability of the model for its purpose. We used the calibrated model to compare the activity patterns and energy budgets of orangutans in both natural and disturbed forests. The results confirm field observations that orangutans in the disturbed forest are more likely to experience deficit energy balance due to traveling to the detriment of feeding time. Such imbalance is more pronounced in males than in females. The finding of a threshold of forest disturbances that affects a significant change in activity and energy budgets suggests potential threats to the orangutan population. Our study introduces the first agent-based model describing the arboreal movement of primates that can serve as a tool to investigate the direct impact of forest changes and disturbances on the behavior of species such as orangutans. Moreover, it demonstrates the suitability of high-performance computing to optimize the calibration of complex agent-based models describing animal behavior at a fine spatio-temporal scale (1-m and 1-s granularity).UKR

Grouping behavior of Sumatran orangutans (Pongo abelii) and Tapanuli orangutans (Pongo tapanuliensis) living in forest with low fruit abundance

In contrast to the African great apes, orangutans (Pongo spp.) are semisolitary: Individuals are often on their own, but form aggregations more often than expected by chance. These temporary aggregations provide social benefits such as mating opportunities. When fruit availability is high, costs of aggregating should be lower, because competition is less pronounced. Therefore, average party size is expected to be higher when fruit availability is high. This hypothesis would also explain why orangutans in highly fruit‐productive habitats on Sumatra are more gregarious than in the usually less productive habitats of Borneo. Here, we describe the aggregation behavior of orangutans in less productive Sumatran habitats (Sikundur and Batang Toru), and compare results with those of previously surveyed field sites. Orangutans in Sikundur were more likely to form parties when fruit availability was higher, but the size of daily parties was not significantly affected by fruit availability. With regard to between‐site comparisons, average party sizes of females and alone time of parous females in Sikundur and Batang Toru were substantially lower than those for two previously surveyed Sumatran sites, and both fall in the range of values for Bornean sites. Our results indicate that the assessment of orangutans on Sumatra as being more social than those on Borneo needs revision. Instead, between‐site differences in sociality seem to reflect differences in average fruit availability

Using Simulation Models to Evaluate Ape Nest Survey Techniques

BACKGROUND: Conservationists frequently use nest count surveys to estimate great ape population densities, yet the accuracy and precision of the resulting estimates are difficult to assess. METHODOLOGY/PRINCIPAL FINDINGS: We used mathematical simulations to model nest building behavior in an orangutan population to compare the quality of the population size estimates produced by two of the commonly used nest count methods, the 'marked recount method' and the 'matrix method.' We found that when observers missed even small proportions of nests in the first survey, the marked recount method produced large overestimates of the population size. Regardless of observer reliability, the matrix method produced substantial overestimates of the population size when surveying effort was low. With high observer reliability, both methods required surveying approximately 0.26% of the study area (0.26 km(2) out of 100 km(2) in this simulation) to achieve an accurate estimate of population size; at or above this sampling effort both methods produced estimates within 33% of the true population size 50% of the time. Both methods showed diminishing returns at survey efforts above 0.26% of the study area. The use of published nest decay estimates derived from other sites resulted in widely varying population size estimates that spanned nearly an entire order of magnitude. The marked recount method proved much better at detecting population declines, detecting 5% declines nearly 80% of the time even in the first year of decline. CONCLUSIONS/SIGNIFICANCE: These results highlight the fact that neither nest surveying method produces highly reliable population size estimates with any reasonable surveying effort, though either method could be used to obtain a gross population size estimate in an area. Conservation managers should determine if the quality of these estimates are worth the money and effort required to produce them, and should generally limit surveying effort to 0.26% of the study area, unless specific management goals require more intensive sampling. Using site- and time- specific nest decay rates (or the marked recount method) are essential for accurate population size estimation. Marked recount survey methods with sufficient sampling effort hold promise for detecting population declines

Sociality predicts orangutan vocal phenotype

In humans, individuals’ social setting determines which and how language is acquired. Social seclusion experiments show that sociality also guides vocal development in songbirds and marmoset monkeys, but absence of similar great ape data has been interpreted as support to saltational notions for language origin, even if such laboratorial protocols are unethical with great apes. Here we characterize the repertoire entropy of orangutan individuals and show that in the wild, different degrees of sociality across populations are associated with different ‘vocal personalities’ in the form of distinct regimes of alarm call variants. In high-density populations, individuals are vocally more original and acoustically unpredictable but new call variants are short lived, whereas individuals in low-density populations are more conformative and acoustically consistent but also exhibit more complex call repertoires. Findings provide non-invasive evidence that sociality predicts vocal phenotype in a wild great ape. They prove false hypotheses that discredit great apes as having hardwired vocal development programmes and non-plastic vocal behaviour. Social settings mould vocal output in hominids besides humans

Raiders of the Lost Bark: Orangutan Foraging Strategies in a Degraded Landscape

Deforestation is rapidly transforming primary forests across the tropics into human-dominated landscapes. Consequently, conservationists need to understand how different taxa respond and adapt to these changes in order to develop appropriate management strategies. Our two year study seeks to determine how wild Sumatran orangutans (Pongo abelii) adapt to living in an isolated agroforest landscape by investigating the sex of crop-raiders related to population demographics, and their temporal variations in feeding behaviour and dietary composition. From focal animal sampling we found that nine identified females raided cultivated fruits more than the four males. Seasonal adaptations were shown through orangutan feeding habits that shifted from being predominantly fruit-based (56% of the total feeding time, then 22% on bark) to the fallback food of bark (44%, then 35% on fruits), when key cultivated resources such as jackfruit (Artocarpus integer), were unavailable. Cultivated fruits were mostly consumed in the afternoon and evening, when farmers had returned home. The finding that females take greater crop-raiding risks than males differs from previous human-primate conflict studies, probably because of the low risks associated (as farmers rarely retaliated) and low intraspecific competition between males. Thus, the behavioral ecology of orangutans living in this human-dominated landscape differs markedly from that in primary forest, where orangutans have a strictly wild food diet, even where primary rainforests directly borders farmland. The importance of wild food availability was clearly illustrated in this study with 21% of the total orangutan feeding time being allocated to feeding on cultivated fruits. As forests are increasingly converted to cultivation, humans and orangutans are predicted to come into conflict more frequently. This study reveals orangutan adaptations for coexisting with humans, e.g. changes in temporal foraging patterns, which should be used for guiding the development of specific human-wildlife conflict mitigation strategies to lessen future crop-raiding and conflicts

Unexpected Ecological Resilience in Bornean Orangutans and Implications for Pulp and Paper Plantation Management

Ecological studies of orangutans have almost exclusively focused on populations living in primary or selectively logged rainforest. The response of orangutans to severe habitat degradation remains therefore poorly understood. Most experts assume that viable populations cannot survive outside undisturbed or slightly disturbed forests. This is a concern because nearly 75% of all orangutans live outside protected areas, where degradation of natural forests is likely to occur, or where these are replaced by planted forests. To improve our understanding of orangutan survival in highly altered forest habitats, we conducted population density surveys in two pulp and paper plantation concessions in East Kalimantan, Indonesia. These plantations consist of areas planted with fast-growing exotics intermixed with stands of highly degraded forests and scrublands. Our rapid surveys indicate unexpectedly high orangutan densities in plantation landscapes dominated by Acacia spp., although it remains unclear whether such landscapes can maintain long-term viable populations. These findings indicate the need to better understand how plantation-dominated landscapes can potentially be incorporated into orangutan conservation planning. Although we emphasize that plantations have less value for overall biodiversity conservation than natural forests, they could potentially boost the chances of orangutan survival. Our findings are based on a relatively short study and various methodological issues need to be addressed, but they suggest that orangutans may be more ecologically flexible than previously thought

Recent Surveys in the Forests of Ulu Segama Malua, Sabah, Malaysia, Show That Orang-utans (P. p. morio) Can Be Maintained in Slightly Logged Forests

BACKGROUND: Today the majority of wild great ape populations are found outside of the network of protected areas in both Africa and Asia, therefore determining if these populations are able to survive in forests that are exploited for timber or other extractive uses and how this is managed, is paramount for their conservation. METHODOLOGY/PRINCIPAL FINDINGS: In 2007, the "Kinabatangan Orang-utan Conservation Project" (KOCP) conducted aerial and ground surveys of orang-utan (Pongo pygmaeus morio) nests in the commercial forest reserves of Ulu Segama Malua (USM) in eastern Sabah, Malaysian Borneo. Compared with previous estimates obtained in 2002, our recent data clearly shows that orang-utan populations can be maintained in forests that have been lightly and sustainably logged. However, forests that are heavily logged or subjected to fast, successive coupes that follow conventional extraction methods, exhibit a decline in orang-utan numbers which will eventually result in localized extinction (the rapid extraction of more than 100 m(3) ha(-1) of timber led to the crash of one of the surveyed sub-populations). Nest distribution in the forests of USM indicates that orang-utans leave areas undergoing active disturbance and take momentarily refuge in surrounding forests that are free of human activity, even if these forests are located above 500 m asl. Displaced individuals will then recolonize the old-logged areas after a period of time, depending on availability of food sources in the regenerating areas. CONCLUSION/SIGNIFICANCE: These results indicate that diligent planning prior to timber extraction and the implementation of reduced-impact logging practices can potentially be compatible with great ape conservation

A small subset of protected areas are a highly significant source of carbon emissions

Protected areas (PAs) aim to protect multiple ecosystem services. However, not all are well protected. For the first time, using published carbon and forest loss maps, we estimate carbon emissions in large forest PAs in tropical countries (N = 2018). We found 36 ± 16 Pg C stored in PA trees, representing 14.5% of all tropical forest biomass carbon. However the PAs lost forest at a mean rate of 0.18% yr(−1) from 2000–2012. Lower protection status areas experienced higher forest losses (e.g. 0.39% yr(−1) in IUCN cat III), yet even highest status areas lost 0.13% yr(−1) (IUCN Cat I). Emissions were not evenly distributed: 80% of emissions derived from 8.3% of PAs (112 ± 49.5 Tg CO(2) yr(−1); n = 171). Unsurprisingly the largest emissions derived from PAs that started with the greatest total forest area; accounting for starting forest area and relating that to carbon lost using a linear model (r(2) = 0.41), we found 1.1% outlying PAs (residuals >2σ; N = 23), representing 1.3% of the total PA forest area, yet causing 27.3% of all PA emissions. These results suggest PAs have been a successful means of protecting biomass carbon, yet a subset causing a disproportionately high share of emissions should be an urgent priority for management interventions

Declining Orangutan Encounter Rates from Wallace to the Present Suggest the Species Was Once More Abundant

BACKGROUND: Bornean orangutans (Pongo pygmaeus) currently occur at low densities and seeing a wild one is a rare event. Compared to present low encounter rates of orangutans, it is striking how many orangutan each day historic collectors like Alfred Russel Wallace were able to shoot continuously over weeks or even months. Does that indicate that some 150 years ago encounter rates with orangutans, or their densities, were higher than now? METHODOLOGY/PRINCIPAL FINDINGS: We test this hypothesis by quantifying encounter rates obtained from hunting accounts, museum collections, and recent field studies, and analysing whether there is a declining trend over time. Logistic regression analyses of our data support such a decline on Borneo between the mid-19th century and the present. Even when controlled for variation in the size of survey and hunting teams and the durations of expeditions, mean daily encounter rates appear to have declined about 6-fold in areas with little or no forest disturbance. CONCLUSIONS/SIGNIFICANCE: This finding has potential consequences for our understanding of orangutans, because it suggests that Bornean orangutans once occurred at higher densities. We explore potential explanations-habitat loss and degradation, hunting, and disease-and conclude that hunting fits the observed patterns best. This suggests that hunting has been underestimated as a key causal factor of orangutan density and distribution, and that species population declines have been more severe than previously estimated based on habitat loss only. Our findings may require us to rethink the biology of orangutans, with much of our ecological understanding possibly being based on field studies of animals living at lower densities than they did historically. Our approach of quantifying species encounter rates from historic data demonstrates that this method can yield valuable information about the ecology and population density of species in the past, providing new insight into species' conservation needs

Tree species that 'live slow, die older' enhance tropical peat swamp restoration : Evidence from a systematic review

Degraded tropical peatlands lack tree cover and are often subject to seasonal flooding and repeated burning. These harsh environments for tree seedlings to survive and grow are therefore challenging to revegetate. Knowledge on species performance from previous plantings represents an important evidence base to help guide future tropical peat swamp forest (TPSF) restoration efforts. We conducted a systematic review of the survival and growth of tree species planted in degraded peatlands across Southeast Asia to examine (1) species differences, (2) the impact of seedling and site treatments on survival and growth and (3) the potential use of plant functional traits to predict seedling survival and growth rates. Planted seedling monitoring data were compiled through a systematic review of journal articles, conference proceedings, reports, theses and unpublished datasets. In total, 94 study-sites were included, spanning three decades from 1988 to 2019, and including 141 indigenous peatland tree and palm species. Accounting for variable planting numbers and monitoring durations, we analysed three measures of survival and growth: (1) final survival weighted by the number of seedlings planted, (2) half-life, that is, duration until 50% mortality and (3) relative growth rates (RGR) corrected for initial planting height of seedlings. Average final survival was 62% and half-life was 33 months across all species, sites and treatments. Species differed significantly in survival and half-life. Seedling and site treatments had small effects with the strongest being higher survival of mycorrhizal fungi inoculated seedlings; lower survival, half-life and RGR when shading seedlings; and lower RGR and higher survival when fertilising seedlings. Leaf nutrient and wood density traits predicted TPSF species survival, but not half-life and RGR. RGR and half-life were negatively correlated, meaning that slower growing species survived for longer. Synthesis and applications. To advance tropical peat swamp reforestation requires expanding the number and replication of species planted and testing treatments by adopting control vs. treatment experimental designs. Species selection should involve slower growing species (e.g. Lophopetalum rigidum, Alstonia spatulata, Madhuca motleyana) that survive for longer and explore screening species based on functional traits associated with nutrient acquisition, flooding tolerance and recovery from fire.Peer reviewe