Our study highlights the importance of considering the impacts of major conservation threats in combination: recent habitat loss and exploitation combine to drive dramatic extinction risks to the forest specialist species of Sundaland. Without urgent policy intervention to curb deforestation and slow the quantities of birds entering the cagebird trade, many species are likely to be lost. Failing to account for these combined threats can lead to a major underestimation of threats in Red List assessments.

Our analysis suggests that exploitation for wildlife trade has caused dramatic declines in many species within the region and underscores the critical role that effectively guarded PAs could play as reservoirs of these species. It remains poorly unknown, however, whether PAs are effective at reducing bird exploitation on the ground and future research should point in this direction. Several factors suggest the impacts of exploitation will continue, including within PAs. First, as popular species become rarer their commercial value will likely increase, accelerating exploitation efforts and declines, potentially resulting in an anthropogenic Allee effect29. Further, as rare species drop out of the market, replacements are often substituted into the market [e.g., the recent emergence of Greater Green Leafbird (Chloropsis sonnerati)25]. Second, unpredictable responses to cultural phenomena can result in previously unexploited species becoming the target of trappers: in Indonesia, the recent popularity of owls is dubbed the ‘Harry Potter effect’30. Third, on-going fragmentation via deforestation and road development into contiguous forest16 (especially in Borneo) will make forest interiors increasingly accessible to trappers, further reducing the number of isolated refugia for commercially valuable species. Recent research suggests that the level of unmapped roads is very high, pointing to increasingly high accessibility of forests for exploitation31. Finally, a lack of funding (annual shortfall of US $521million per year in Indonesia) for patrols and insufficient law enforcement and punishment of exploitation means that many PAs do not effectively prevent trapping and hunting7,19,26,32. This is particularly concerning given that all of the regionally endemic, persecuted species have below 10% of their range within the core of a PA (i.e., >5 km from an edge). Thus, PAs will likely only protect the subset of non-persecuted species by potentially reducing habitat loss and they may fail to prevent extinctions of many commercially valuable species.

Our study also underscores the importance of deforestation as an extinction driver. Forest loss, largely due to the expansion of agriculture, has a direct negative impact on the majority of forest species within the region, and this reduction is on-going in Sumatra, Borneo, and Peninsular Malaysia33,34.

Previous analyses have used a reverse species-area relationship to predict the direct impact of deforestation on extinction risk in the region, estimating that between 24 and 42% of all biodiversity faces extinction12,35 (but see He & Hubbell36). Our results are somewhat lower [16.9% (52 species)—30.1% (92)] likely reflecting an increase in the accuracy of remote sensing analyses from previous studies. However, our figures do not include the additional extinction risks posed by hunting and trading of commercially valuable species (Supplementary Figure 3).

While considerable debate surrounds the actual rate of extinctions solely from habitat loss36,37, in combination, habitat loss, and hunting have resulted in numerous extinctions globally at both the island (e.g., Mascerenes38) and continental (e.g., megafaunal extinctions in the Late Quaternary39) scales. Given the particularly acute nature of these threats in Sundaland, without concerted conservation efforts to greatly reduce deforestation and exploitation, the region is at significant risk of being an extinction hotspot in the future.

While our method is a rapid and straightforward way for assessing population declines, there are several limitations that must be noted. In assessing the impact of exploitation, detailed information on the behaviour of wild bird trappers and species responses to exploitation is not available. Hence, we made simplified assumptions regarding hunting impact and accessibility, but in reality, species responses to hunting are more nuanced than the three categories we used (low, medium, and high)40 and accessibility is a complex interaction of population, roads, topography, and markets. We attempted to account for this uncertainty by combining maps of major roads and all available roads to calculate additional metrics of accessibility. Using road maps instead of forest edges made considerable difference to our results, with both road maps leading to considerably lower threat estimates.

Using only major roads only 16 species were above Red List thresholds (6 EN and 10VU) and with all roads 38 (3 CR, 13 EN, 22 VU) (Supplementary Figure 4 and Supplementary Figure 5). However, the maps we used, while the best available (Open Street Map and WRI produced Indonesia map), are fundamentally inaccurate with many roads missing31,41. Crucially, this inaccuracy is not uniform and changes the analysis in biased and unpredictable ways. For example, the maps contain no roads inside protected areas in Java, suggesting Javanese forests are much more isolated than they actually are, leading to large underestimations of threat. Second, deciding to what extent individual roads are accessible to hunters requires further assumptions. By using distance from forest edge we avoid using maps that are known to be inaccurate41 and we can account for access from other means (such as rivers) by assuming deforestation follows these points of access.

Because our knowledge of trade dynamics and trapper behaviour is best in Indonesia, we made the conservative assumption that there was no exploitation outside Indonesia, but this is certainly not the case for many species24,25 and—at worst—led to unrealistic estimates in globally endangered species that are either highly persecuted outside of Indonesia (e.g., Straw-headed Bulbul, Pycnonotus zeylanicus25) and/or have the majority of their range in Malaysia (e.g. Malay Peacock-pheasant, Polyplectron malacense). Despite these limitations, our results agree with a recent meta-analysis of hunting, which showed global average population declines of 58% (versus 36.6% in this study), and depletion within 7 km of access points, further highlighting the role of the pet trade in driving defaunation7,42.

In predicting losses to deforestation, the underlying maps, while the best available, likely contain commission and omission errors (e.g., areas that are either included or excluded erroneously), which could lead to inaccurate decline or exploitation estimates. The changes in mapping methodology outlined in the methods also led to conservative/underestimates of ESH decline, at its most extreme 23 species (Javanese endemics and range restricted Island species) experienced an increase in ESH between 2000 and 2015. However, all the species affected are restricted to extremely limited extents and hence, have likely remained largely unchanged in the analysis period. We therefore do not expect any substantial population increases in these species, instead the increases highlight how our estimated decreases in other species are likely conservative.

Also, inaccuracies may occur where species’ habitat requirements are not fully understood [e.g., Bonaparte’s Nightjar (Caprimulgus concretus)]. Our method is not sensitive to species that have very specialised habitat requirements, or exist at very low densities within suitable habitat. For example, the Javan Blue-banded Kingfisher (Alcedo euryzona), which is limited to lowland and hill riverine forest that is not specifically defined on our maps, is suggested to be downgraded from CR to LC in our analysis, but riverine forest has been particularly affected by deforestation in the region43. Consequently, while our results represent an improvement on existing knowledge in the majority of cases, each assessment must be judged in context, as would occur in any normal IUCN assessment process.

We also assume a linear relationship between deforestation and population decline, which we believe is a conservative assumption given the negative impacts that edge, area and isolation effects have on species44. There is considerable debate as to whether the relationship is linear, with many theoretical (and some field) studies suggesting that populations can remain reasonably stable until a certain threshold of habitat loss (for a comprehensive review see Swift and Hannon45), leading to overestimates of population decline under linear assumptions. However, while habitat thresholds may exist for some species in our study, given our current knowledge, calculating these thresholds accurately is impossible and as such they cannot be incorporated into our analysis and would be of questionable utility to conservation decisions45. Instead, our assumption of linearity is in line with the precautionary principle (which is acknowledged in the Convention of Biological Diversity), since it ensures we are not under-estimating declines by assuming a threshold that does not exist, and thus is more useful to conservation decisions. For simplicity, we also assumed that the effects of the loss of habitat from deforestation and exploitation were additive, which results in three species having maximum estimated declines above 100%. In reality, the proportion of the remaining area of a species subjected to exploitation will increase as the habitat is reduced and fragmented, meaning the impacts are likely synergistic46, making our estimates for most species conservative.

Our results suggest that by failing to account for the combined impacts of habitat loss and exploitation, the Red List currently underestimates the threats facing many species. By incorporating quantitative measurements of habitat loss and exploitation, our Red List assessments differed substantially from the current IUCN status. Currently, only 27 species in the region are Red listed (VU, EN, or CR), whereas our results indicate that this should increase by more than 80% to 51 species, but only if deforestation and exploitation threats are considered together. By incorporating exploitation impacts within spatial assessments of edge effects, we have identified species that are likely suffering precipitous, undocumented population declines.

In this study, we estimated the rates of population decline over 3 generations or 10 years, for assessment under the IUCN criteria A3 using an index of abundance and actual levels of persecution. The mode of assessment applied can make a significant difference to the end result. In our case, criteria E (a quantitative assessment of extinction risk) could be used via a species-area relationship calculation, but we chose not to use this method because the SAR has been previously criticised for over-estimating extinction risk from habitat loss36. However, future reassessments using this criterion and more complicated extinction-risk models are a valuable area for future research.

While we assessed two major threats in combination, we did not consider other threats, such as the impacts of logging, which will likely cause substantial reductions in some species. In Malaysian Borneo, for instance, 92 of our study species suffered from reduced abundance following intensive selective logging47. Given the vast majority of lowland forest remaining in the region has been selectively logged48, our Red List assessments are probably conservative for many species. We did not incorporate logging effects into our assessment because the impacts on many species remain unknown (especially those restricted to Java and Sumatra). The same is also true for the impacts of increasing fragmentation, which we do not directly consider, but are likely to have profound implications for many species44. Incorporating logging impacts and fragmentation effects represents another important frontier in combined species assessment, especially in logging ravaged regions in the tropics (i.e., Southeast Asia, Congo, Southern, and Eastern Amazon).

Another key issue, with profound implications for conservation designation, is where the limits are drawn for full species status. For example, there is controversy surrounding the taxonomic treatment used by the IUCN Red List for birds49. Five recently suggested elevations of sub-species to full species status50 in the region are not recognised by the IUCN, with at least one species qualifying as CR [Barusan Shama (Copsychus melanurus)), one as EN (Enggano Parakeet (Psittacula modesta)) and another as VU (Brown Wood Owl (Strix indranee)] by our estimation. This discrepancy emphasizes how the blanket application of a single taxonomic treatment can exacerbate the underestimation of threats facing biodiversity in Red List assessments50,51, suggesting that conservation would benefit from mechanisms to assess extinction risk under alternative taxonomic treatments on the IUCN Red List.

In conclusion, our results uniquely highlight the precipitous declines of many Sundaic forest-dependent birds over the last 15 years from the combined impacts of rapid deforestation and exploitation and, as a result, that current IUCN Red List assessments underestimate threats in the region. For commercially valuable species, wildlife trade is the leading cause of decline in the majority of cases, yet very little information is available on the dynamics of trade, the behaviour of trappers, and in turn, population responses of traded species, indicating an urgent research need26,52. While a slowing of deforestation is essential to limit extinctions of forest-dependent birds, without coordinated efforts to curb commercial exploitation, including better protection in PAs and stronger law enforcement, numerous extinctions of commercially valuable species appear inevitable. Finally, the combined impacts of deforestation, forest fragmentation and commercial exploitation are not unique to Southeast Asia; for example, rampant land-use change and wildlife trade drives declines in parrots from Latin America, Africa, and mainland Asia53,54. Therefore, the extinction risks from deforestation and exploitation may be severely underestimated globally, making it essential for future quantitative conservation assessments to take into account the combined effects of habitat loss, hunting, and exploitation.