Encounter rates and densities

It is suggested herein there has been a decline in orangutan encounter rates on Borneo between the mid 19^th century and the present, with mean daily encounter rates appearing to have declined about 6-fold in areas with little or no forest disturbance. We do not know whether this indicates a decrease in orangutan densities of the same magnitude, because encounter rates and densities may not be linearly related. For example, if orangutans that occur at higher densities tended to exhibit a more clumped distribution (e.g., due to aggregation around high quality food resources), then encounter rates may increase exponentially at high population densities. There is some support of decreasing maximum group size, with two historic hunters reporting encountering groups of 7 animals [5], [20]. Such group sizes have not been reported on Borneo in recent times, although 4 respondents reported seeing 5 animals together. Without further information on the relationship between encounter rates and densities it is not possible to estimate historic densities of orangutans.

Possible sources of bias

We recognize that the data have limitations, and the various biases that are introduced by comparing historic literature and museums records to recent field surveys are caveats to any of our conclusions. Some possible sources of bias such as the different durations and different sizes of expeditions are easily identified and, when these variables are known, can be included as parameters in our models. Other sources of bias are less easy to remove.

One obvious question is whether historic hunting and surveying methods are similar enough to present-day surveys to warrant comparison. Museum collectors used local trackers to find and shoot orangutans and other species, or to notify the collectors of the presence of orangutans so that the collectors could shoot them. Surveyors, both recent and historic, would walk through a forest area and note the orangutans they encountered. The focus in present-day transect surveys is often on orangutan nests rather than the animal itself, and this method may reduce the chance of orangutan encounters. To test for this effect, we subsampled our data and only selected those recent surveys in which the specific purpose was to sample quietly a forest area with a team of surveyors and count directly as many orangutans as possible. Nine surveys in different parts of Borneo between 2002 and 2009, involving 724 surveys days, resulted in the detection of 108 orangutans, or a daily encounter rate of 0.18 (SD = 0.22). This is about double the estimated average encounter rate for recent surveys based on the full data set (0.08), suggesting that normal nest transect surveys reduce the likelihood of encountering orangutans. Still, this estimate is three times lower than the historic encounter rates, even though the detection methods are similar.

Under-reporting of non-encounters with orangutans is another possible source of bias. Hunters mostly focused their collection activities in the areas with the highest densities, primarily the swampy lowlands [20], but hunters working in areas with low orangutan densities might have encountered very few or no orangutans and would rarely record such missing records, although during recent surveys such zero-encounters are commonly reported. Our separate analyses of encounters/non-encounters and conditional abundance (given at least one detection) allow us to reach some conclusions that are not affected by the possibility of changes in the pattern of underreporting non-encounters. The statistically significant outcomes of linear regression of non-zero encounter data, indicates that there is an overall decline in the numbers of detected orangutans, irrespective of possible biases in reporting non-encounters.

Possible causes of declining orangutan encounter rates

A possible explanation for lower encounter rates in recent times is that because of increased frequency of encounters between people and orangutans, orangutans are now more elusive and have learned to avoid people. This would especially be the case if orangutans had learned to consider humans as a serious threat. Descriptions by Wallace [4] or Beccari [5] do suggest that orangutans were less likely to flee when they encountered humans than unhabituated orangutans encountered in the 21^st century. There is also some indication, although not substantiated by data, that in areas where orangutans have not been hunted for a long time, such as the Kinabatangan area in Malaysian Borneo, they tend to be easier to see than in areas where hunting still occurs. Still, because orangutans are not group living there is little to learn from other group members being shot. And also, because of their size and slow movement, orangutans have a high chance of being killed once spotted. Such characteristics would make it less likely that orangutans would learn to actively avoid people. A more detailed analysis of descriptions of both recent and historic orangutan encounters might reveal whether behavioural changes have indeed occurred. We doubt, however, that such changes could fully account for the observed decrease in encounter rates.

A more likely explanation for decreased encounter rates is that the local densities of orangutans have actually declined. This leads to the question of what would have caused this decline. We investigate the major causes of orangutan decline to assess how they relate to the observed decline in encounter rates: habitat loss and degradation, hunting, and disease.

Although we avoided using disturbed sites in the analysis, it is possible that overall forest disturbance around sites surveyed in the 19^th century was lower than in the late 20^th and 21^st. Deforestation has disproportionately affected lowland forests and orangutans disproportionately favor such habitats. If the 19^th-century expeditions had focused on lowland forests, while modern fieldwork focused on Borneo's only remaining lightly-affected forests—those in the higher elevation interior—a decrease in encounter rates would also have been observed. Such a geographical shift is not obvious, however, with the focus in both pre- and post-deforestation surveys (with cut-off year 1965) being on coastal lowlands (Fig. 3). Also, if large-scale deforestation and forest degradation caused the observed differences in encounter rates, we would expect to see a sudden decline in encounter rates after the 1960s and 1970s, coincident with major intensification of these activities during this period. Our data suggest a decrease in orangutan encounter rates at least from the early 19^th century onward, some 120 years before major deforestation started [21], [22]. Unfortunately, we do not have enough data from the period 1900–1960/1970, to specifically test whether the decrease in encounter rates became more severe after large-scale deforestation started. What we do know, however, is that although orangutan numbers generally decrease following habitat disturbance [3], they do manage to survive in high densities in some areas that have been heavily disturbed or even clear-cut and planted with monocultural plantations [23]. We think therefore that the decline in encounter rates could not have been caused by reduced habitat quality alone, and that other factors need to be explored.

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Figure 3. Map of Borneo with locations of surveys.

The location of orangutan surveys conducted before (black symbols) and after (red symbols) large scale deforestation started (with cut-off year 1965), in relation to the upland areas of Borneo (indicated by the grey area in the centre of the island). Location symbols are scaled to daily encounter rates, with smallest symbol representing encounter rate = 0; next size, between 0 and 0.05; next size, between 0.05 and 0.22; and largest symbol, >0.22.

https://doi.org/10.1371/journal.pone.0012042.g003

Hunting orangutans for meat or as agricultural pests remains common in most parts of Borneo, as shown from Borneo-wide surveys in the mid-1990s and 2008 [13], [24]. Because of teir low fecundity orangutans are very sensitive to hunting, and population viability models suggest that any population will go extinct eventually if hunting increases annual adult mortality by >1% [25]. Such local extinctions have been demonstrated by Pleistocene and Holocene orangutan remains found in caves in parts of Borneo where orangutans no longer occur, although suitable habitat remains [26], [27]. In fact, thousands of orangutan teeth found in sub-recent deposits in areas where orangutans had become extinct by historic times (Niah in north-western Borneo, and Padang in central Sumatra) suggest that orangutans were as commonly hunted as the ubiquitous wild pigs. Thus, in many areas, orangutans had already become extinct or reduced to very low population levels by the time of the first orangutan distribution assessments in the 19^th century. Spatial patterns show that local extinctions of orangutan populations that occurred before the time of the first descriptions of their ranges had primarily occurred in areas with nomadic human societies [13]. These people generally roam in upland areas with poor soils where permanent agriculture is difficult to maintain. The effective hunting ranges of these nomadic people were large, as opposed to settled agriculturalists that would have mostly hunted near their village and had less time to hunt. A combination of reduced carrying capacity in upland forests because of lower soil fertility, and higher hunting pressure may be an important explanation why orangutans became locally extinct in extensive dryland forest areas of Borneo during pre-historic times.

As opposed to dryland forests, freshwater and peat swamp environments of Borneo were virtually uninhabited by people until the 19^th century when commercial extraction of wood and forest products started [21]. Thus, we assume that these environments contained the majority of orangutans, not necessarily because these were ecologically more suitable, but rather because hunting in swamps had been rare or absent until the late 18^th and early 19^th century. These swamps are also the areas where most collecting during the 19^th century occurred (Fig. 3). We hypothesize that, once swamp areas started to be exploited commercially and human population densities increased, hunting of orangutans by local people as well as trophy collectors, and later for the pet trade, reduced densities in swamp habitats resulting in the observed reduced encounter rates.

The above hunting scenario is supported by genetic analyses of orangutan populations in the Malaysian state of Sabah, which strongly suggest that a decline in Sabah's orangutan populations of at least one order of magnitude most likely occurred within the last one or two centuries [28]. It is shown that the decline has been very recent and sharper than generally assumed. The current orangutan distribution in Sabah is also strongly related to the distribution of hunter-gatherers tribes according to interview data (MA unpubl. data). Orangutans are absent from most of the western side of the state where, until recently, they were heavily hunted for meat or traditional medicine, but they are common in the eastern forests of the state, that are either not inhabited or occupied by tribes with no primate hunting tradition. It remains unclear why hunting pressure would have increased in western Sabah a few hundred years ago. The timing coincides with the approximate end of head-hunting in Borneo, which had kept large parts of the island too dangerous to travel in [29], [30]. Banks [31] inferred that head-hunting provided wildlife a refuge, because large areas of forest were avoided by hunters fearful of roving bands of head-hunters. He noted that, immediately after the colonial ban on head-hunting was enforced, many forest areas became much safer to travel through, allowing hunters to travel further from villages, and leading to the rapid demise of, for example, the Sumatran rhinoceros Dicerorhinus sumatrensis. Also, it has been suggested that orangutan heads replaced human heads as trophies [32], which may also have added to hunting pressure on orangutans.

Hunting-related distribution patterns of orangutans have also been noted in the Indonesian part of Borneo. Te Wechel [33] reported that in the early 20^th century around the lower Barito River in southern Borneo, orangutans were rarely seen near villages, but remained common in the inaccessible swamps away from the rivers. In the same region, Lumholtz [29] found that in the lower reaches of the rivers almost no one lived and that orangutans were more common, as judged by their frequent calls and sightings. Further upriver, however, towards the centre of Borneo, people were more common and orangutans rare. More recent surveys have reported similar patterns: distance to the nearest village known to hunt orangutans is the strongest predictor of orangutan population density [34].

A final possible cause of density declines and encounter rates is disease. Orangutans suffer from a range of diseases, many of which also affect people [35]. Even though such disease can have high mortality rates on animals in captivity, there are no documented cases of disease epidemics in wild orangutan populations. With increasingly-frequent human-orangutan contact caused by shrinking habitat extent, we cannot exclude disease as a possible contributing factor to overall declining densities. Still, without any supporting evidence of disease as a major threat to wild orangutans we do not think it has played a major role in the observed encounter rate trends.

Recommendations for management and research

This study would have benefited if both historic and recent encounter rate data had been available from the same localities. We cannot claim to have found all relevant survey and collection data and urge others to search for areas for which there are both good historic and recent reports on orangutan encounters. To determine the relationship between encounter rates and densities, it would be useful to design a survey covering areas of high, medium and low orangutan densities (as determined by formal line transect methods) in which reconnaissance walks are done specifically to find wild orangutans. Such data would allow an estimation of historic orangutan densities.

The findings in this paper could change our view of orangutans, because it is suggested that many Bornean populations could presently occur at densities well below those that would be imposed by food availability (i.e., densities are below the ecological carrying capacity). This suggests that some behavioural information on orangutans is biased by the fact that such populations were not studied at carrying capacity. We do not know enough about the ecological and behavioural flexibility of orangutans to predict how the species would react to significant density suppression, but we recommend that researchers keep this idea in mind when they study orangutans: How would the species behave if natural densities were 10 animals/km²? There is a need to interpret orangutan behaviour and ecology in the light of these new insights. To understand better how orangutan behaviour is affected by density, lessons could be learned from situations where orangutans exist in high densities, such as the fragmented populations of the Kinabatangan River in Malaysian Borneo. Comparative studies of breeding behaviour and social interactions in different density settings, and under different historic and present hunting regimes, may provide further insights into the ecology of orangutans under optimal ecological conditions. In turn, this would provide useful input into management of both in-situ and ex-situ populations.

Conclusion

The usefulness of historic literature data for assessing population trends of threatened species is shown, not just by mapping historic ranges, but through estimation of encounter or catch rates. Even though statistical noise and bias are unavoidable in such assessments, the insights they provide may considerably change our views on the ecology of species and how to prevent their extinction. We hope that such studies are stimulated by this paper.