- Email: [email protected]
Threats to the populations of two endemic brushturkey species in Indonesian New Guinea
Journal of Asia-Pacific Biodiversity xxx (xxxx) xxx
Contents lists available at ScienceDirect
Journal of Asia-Pacific Biodiversity journal homepage: http://www.elsevier.com/locate/japb
Original Article
Threats to the populations of two endemic brushturkey species in Indonesian New Guinea Margaretha Z. Pangau-Adam a, *, Jedediah F. Brodie b a b
Department of Conservation Biology, Institute of Zoology and Anthropology, University of Göttingen, 37073, Göttingen, Germany Division of Biological Sciences & Wildlife Biology Program, University of Montana, Missoula, MT, 59812, United States
a r t i c l e i n f o
a b s t r a c t
Article history: Received 19 November 2018 Received in revised form 30 April 2019 Accepted 13 July 2019 Available online xxx
Half of megapode bird species occur in New Guinea and adjacent islands, and almost all of the species are endemic to this region. Despite rapid regional development and deforestation in New Guinea, little is known about the population ecology of these birds, many of which are threatened or endangered. We used camera traps to assess impacts of anthropogenic disturbance and introduced predators on the occurrence and local abundance of red-legged brushturkey Talegalla jobiensis in lowland forests of Nimbokrang, Papua, and the wattled brushturkey Aepypodius arfakianus in the Arfak mountains, West Papua, Indonesia. In hierarchical occupancy models, detection rates were higher in logged forest for both brushturkey species. Occurrence rates of brushturkeys were not affected by logging, hunting pressure, or pig abundance. However, as degradation of megapode habitat is increasing across New Guinea, it is predicted that concurrent pressures from two or more of these threats could affect the distribution and populations of brushturkeys. Ó 2019 National Science Museum of Korea (NSMK) and Korea National Arboretum (KNA), Publishing Services by Elsevier. This is an open access article under the CC BY-NC-ND license (http:// creativecommons.org/licenses/by-nc-nd/4.0/).
Keywords: Endemic birds Hunting Logging Megapodes Papua
Introduction The family of megapode birds (Megapodiidae) is confined to the Indo-Pacific and distributed mainly in New Guinea, where 11 of the 22 species occur (Pratt and Beehler 2015). These birds have a highly unique breeding biology, where they incubate their eggs using heat from environment sources (solar energy, volcanic activity, and microbial decomposition) and where the chicks are entirely independent after hatching (Frith 1956, Jones et al 1995). In New Guinea, megapodes bury their eggs in large mounds that they build of compost, which generate heat for egg incubation from decaying organic materials (Jones et al 1995, Sinclair 2007). Many megapodes are threatened with extinction. Over half of the species that once existed in Oceania are now extinct (Steadman 2006), and almost half of the remaining species are classified by the IUCN as threatened and exhibiting population decline (Sinclair 2007) because of habitat destruction, hunting, collection of eggs,
* Corresponding author. Biology Department, Faculty of Natural Sciences and Mathematics, Cenderawasih University, Jayapura Papua, Indonesia. E-mail addresses: [email protected] (M.Z. Pangau-Adam), jedediah.brodie@ gmail.com (J.F. Brodie). Peer review under responsibility of National Science Museum of Korea (NSMK) and Korea National Arboretum (KNA).
and introduced predators (Dekker et al 2000, IUCN 2016). A recent study reported that because of their unique ecological traits, megapodes may also be vulnerable to climate change (Radley et al 2018), possibly exacerbated by other anthropogenic threats (Brook et al 2008). In spite of the high number of megapode species occurring in New Guinea and adjacent islands, there is a lack of data on the distribution and status of megapodes there. We studied a population of red-legged brushturkey Talegalla jobiensis in lowland forests and a population of wattled brushturkey Aepypodius arfakianus in submontane forests of Papua, Indonesia, using motion-triggered camera traps. Both species are endemic to New Guinea and adjacent islands and sympatric in lower montane forests (Pratt and Beehler 2015). Wattled brushturkey inhabit the upland interior forests of the mountains of New Guinea, and red-legged brushturkey are in lowland to mid-montane forests of northern New Guinea. These brushturkeys are among the least studied and poorly known megapodes, especially with respect to their population ecology. Although both of the brushturkey species have wide distributions and they were recently classified as Least Concern on the IUCN Red List (BirdLife International 2012, 2016), increasing deforestation and habitat loss may considerably threaten their populations. Rapid regional development and growing human
https://doi.org/10.1016/j.japb.2019.07.005 pISSN2287-884X eISSN2287-9544/Ó 2019 National Science Museum of Korea (NSMK) and Korea National Arboretum (KNA), Publishing Services by Elsevier. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Please cite this article as: Pangau-Adam MZ, Brodie JF, Threats to the populations of two endemic brushturkey species in Indonesian New Guinea, Journal of Asia-Pacific Biodiversity, https://doi.org/10.1016/j.japb.2019.07.005
2
MZ Pangau-Adam, JF Brodie / Journal of Asia-Pacific Biodiversity xxx (xxxx) xxx
populations in Papua have driven the conversion of large forest areas to agricultural lands, settlements, and infrastructure. This is accompanied by logging activities that are increasing rapidly in the region, as concession companies have shifted their interest to New Guinea following the collapse of timber stocks in other parts of Indonesia. Habitat disturbance is considered among the major threats to brushturkeys and can lead to fragmentation of the species’ ranges (Dekker et al 2000). Even short of complete deforestation, selective logging can degrade the forest, reducing the quality of habitat for brushturkeys that need leaf litter for their nest mounds. Bird capture and harvesting of eggs are also serious threats to brushturkeys and other megapodes. Because their nest mounds are large and conspicuous, these are easily found by humans and other predators (Sinclair 2007). Many megapode species including brushturkeys spend long periods of time at their incubation sites (Jones et al 1995); therefore, snaring and hunting of adult birds are widespread in New Guinea (Mack and West 2005, Pangau-Adam and Noske 2010). Because brushturkeys lay substantial clutches of eggs that are large and have a high yolk content (Dekker and Wattle 1987), egg collecting is a useful expenditure of time and energy for their predators, including humans (Sinclair 2007). Unsustainable egg harvesting has led to the abandonment of nesting fields and local extinctions of some megapodes in Indonesia (Argeloo and Dekker 1996, Baker and Butchart 2000, Dekker et al 2000). Although hunting of wildlife in Papua is not prohibited, the Indonesian government has ratified laws for the protection of a number of wildlife species (Government of Indonesia Regulation No. 7 1999), and megapodes are among the protected birds. However, illegal hunting and egg collecting are still widespread (PangauAdam pers. observation). Another potential threat to brushturkeys is introduced predators. Mammal introductions in New Guinea are of conservation concern because the region lacks many placental mammal lineages. Invasive species may become an added stressor with multiple other threats such as habitat change (Doherty et al 2015). Invasive primates near Jayapura, Papua, for example, mainly inhabit fragmented forests (Kemp & Burnett 2007), and they could have significant effects on native birds that are not adapted to these nest predators (Corlett and Primack 2011), especially on forest birds facing habitat changes. There were no ungulates in New Guinea before the introduction of pigs (Sus scrofa S. celebensis) by humans thousands of years ago (Flannery 1995). Pigs are known predators on both adult megapodes and their eggs (MacKinnon 1981). As they breed quickly and are omnivorous, pigs may also affect the population and persistence of brushturkeys in New Guinea. The aim of this study was to determine whether the occurrence rates of two brushturkey species were affected by logging, hunting, and introduced pigs, while accounting for natural variation in occurrence driven by elevation and forest structure. Material and methods Study areas Fieldwork was conducted at two humid tropical forest areas, (1) in the lowlands near Nimbokrang, Papua Province and (2) in the Arfak Mountains, West Papua Province (Figure 1). The Nimbokrang lowlands comprise a mosaic of forest habitats including large portions of intact forest. The site has flat alluvial forest, much of which was flooded to a depth of a few centimeters at the time of survey. Typical canopy tree genera are Instia, Pometia, Ficus, Canarium, Alstonia, and Terminalia, while understory trees include Myristica, Syzygium, Garcinia, Diospyros, Pandanus, and palms. Large areas of
the forest are claimed as traditional or clan forest by the local people, with several different land use systems such as shifting cultivation and forest gardens. The forests have not been commercially logged, although illegal selective logging of merbau Intsia bijuga (Fabaceae) is widespread. The Arfak Mountains are one of the protected areas in West Papua, located about 35 km from the capital city of the Province, Manokwari. The topography is steep and the forests have a lower canopy than in Nimbokrang and denser understorey vegetation. There has been no commercial logging, and forest clearance for small-scale subsistence agriculture and for house construction are limited to areas near villages. The wattled brushturkey is the only megapode that inhabits this area. Field sampling In June 2014, 20 camera trap stations were set out at each study site. Reconyx HC500 camera-traps (Reconyx, Inc. Holmen, USA) were installed along transects radiating from two villages in each site. The sampling area in Nimbokrang was at 15e660 m elevation in lowland alluvial forest, and in the Arfak Mountains was at 1,030e 2,280 m elevation in lower montane forests (Flannery 1995). Cameras were deployed c. 1 km apart along each transect, usually on small game trails, stream beds, ridge tops, or in other areas that animals might use for movement or foraging. The distance from the cameras to human habitation or roads was 0.2-6 km, with various distance categories approximately equally represented. Cameras were attached to the bases of trees and housed within protective metal cases. They operated 24 hours per day, recording colour images during the day and black-and-white at night. When triggered by motion in front of the receptor, the camera recorded a sequence of three images and then did not record again for at least 30 s. All cameras in both sites were retrieved 5e7 months later. Data analysis We used hierarchical occupancy models (MacKenzie et al. 2005) to assess the response of brushturkeys to human disturbance in the form of logging, hunting, and introduced invasive pigs. These models are widely used to analyze data from camera traps and allow the robust estimation of occupancy probabilities while accounting for imperfect detection. Specifically, occupancy models partition variance in the data between an occupancy function and a detectability function, with covariates potentially applied to both. We used 5-day sampling intervals at each camera stationdas in other studies (e.g. Brodie et al 2014). This served to reduce the number of zeroes (i.e. sampling intervals without any detections) in the data; data sets with excessive numbers of zeroes, a common problem when surveying rare and elusive rainforest animals, can be problematic for model convergence and parameter estimation. To assess the study objective, we ran occupancy models with covariates for logging, hunting, and relative pig abundance. The logging term (logged) was binary, indicating whether or not the forest around the camera station had been selectively logged. As a proxy for hunting pressure, we used a Geographic Information System to measure the distance from each camera station to the nearest road or town (distance). This metric has been demonstrated to strongly predict vertebrate diversity and biomass across tropical systems (Benitez-Lopez et al 2017). As a metric of pig relative abundance (pig) at each camera station, we used the number of photographic captures of pigs per 100 trap days. Because brushturkey occupancy could also be affected by natural variation in the ecosystem, we included additional covariates that served as proxies for forest structure and abiotic conditions
Please cite this article as: Pangau-Adam MZ, Brodie JF, Threats to the populations of two endemic brushturkey species in Indonesian New Guinea, Journal of Asia-Pacific Biodiversity, https://doi.org/10.1016/j.japb.2019.07.005
MZ Pangau-Adam, JF Brodie / Journal of Asia-Pacific Biodiversity xxx (xxxx) xxx
3
Figure 1. The study sites in the Arfak Mountains (West Papua Province) and Nimbokrang (Papua Province) in Indonesian New Guinea.
(e.g. temperature), namely elevation and forest height. Elevation is the strongest determinant of forest structure, tree species composition, and temperature in this region (Corlett 2009). We measured elevation in the field using a Garmin 64S Global Positioning System unit with an internal barometric altimeter. Forest height was taken from a global map of tropical forest canopies (Simard et al 2011). We considered three detection covariates. First, we assessed whether detection varied between logged and unlogged forest, as logging can induce changes in understory structure that might affect camera visibility or animal movement behaviors. Second, we included the number of days since camera deployment (time) as a sampling covariate, as animals might avoid or be attracted to camera stations initially based on recent human presence (Brodie et al 2014). Finally, we included the total number of hours that each camera was deployed for at each station (camhours)dthis was 120 h (24 h d-1 5 d) for most sampling intervals but usually less for the last interval. Because of the number of covariates that we wished to examine, we could not assess all possible combinations of factors, partly because the model set would have been extremely large and also because, with our relatively sparse data, highly parameterized models did not converge. So we used a sequential process of selecting models. First, we chose the best detection variable by examining four models, one for each detection covariate plus an intercept-only model. Each of these four models included all of the occupancy variables. We chose the variable in the model with the lowest Akaike Information Criterion (AIC) as the detection covariate. Next, we used a backwards-selection stepwise procedure to
identify the most parsimonious occupancy covariates. We started with a global model that included the detection covariate and all of the occupancy covariates and sequentially removed occupancy variables with the lowest absolute value z-statistics until the AIC was minimized. Finally, we compared this top model to a null model with the detection covariate but only a model intercept in the occupancy function. We used model averaging between the most parsimonious model and the null model for multimodel inference. We assessed multicollinearity among predictor variables before model analysis and did not include variables with jrj > 0.7 in the same model. We analyzed the two brushturkey species separately and also by pooling their data to determine general patterns that affected both (while also increasing the sample size and thus statistical power). For the combined-species analysis, we did not include elevation or forest height covariates as these differed so greatly between the study areas. Results Several camera traps at each location were stolen. Out of a total of 2211 sampling days across 16 camera stations in the Arfak Mountains and 2433 sampling days across 12 stations in Nimbokrang, we obtained 31 detections of wattled brushturkeys and 19 detections of red-legged brushturkeys. For the red-legged brushturkey, logged was the best detection covariate, with detection rate being higher in logged forest. After stepwise variable selection, the most parsimonious model included
Please cite this article as: Pangau-Adam MZ, Brodie JF, Threats to the populations of two endemic brushturkey species in Indonesian New Guinea, Journal of Asia-Pacific Biodiversity, https://doi.org/10.1016/j.japb.2019.07.005
4
MZ Pangau-Adam, JF Brodie / Journal of Asia-Pacific Biodiversity xxx (xxxx) xxx
positive effects of elevation, logging, and pig relative abundance, and a negative effect of distance to the nearest road or village, on brushturkey occupancy. For all of the occupancy variables, the standard error (SE) exceeded the parameter coefficient in magnitude, indicative of a very weak (at best) effect. Moreover, the top model was w1.5 AIC units worse than the intercept-only model (Table 1). For the wattled brushturkey, logged was the best detection covariate, with detection rate being higher in logged forest. Forest height and elevation were correlated (r ¼ 0.73), and so only the latter was included in subsequent models, as it had a much greater range of variation than the former. The most parsimonious occupancy model included a positive effect of distance to the nearest road or village on occupancy, but the SE was larger than the coefficient, and the model was w3 AIC units worse than the interceptonly model (Table 1). For the two species combined, no detection covariate outperformed the intercept-only detection model. The most parsimonious occupancy model included a positive effect of distance to the nearest road or village on occupancy, but the SE was larger than the coefficient, and the model was w2 AIC units worse than the intercept-only model (Table 1). Based on the best-performing, intercept-only detection models, the average proportion of each study area occupied by brushturkeys (i.e. the model intercept) was 0.21 (SE ¼ 0.66) for red-legged brushturkeys in Nimbokrang and 0.70 (0.60) for wattled brushturkeys in the Arfak Mountains. Discussion This is the first assessment on the population ecology and factors influencing occurrence of the red-legged brushturkey and the wattled brushturkey in Indonesian New Guinea. Although hunting and egg harvesting are common threats to megapodes (Jones et al 1995, Dekker et al 2000), we did not detect an effect of potential hunting pressure (distance to roads and villages) on occurrence rates of brushturkey. It may be that the roads and towns in the study areas were too small, or the human density too low, to see these effects, or that hunters simply ranged very widely (>6 km, the maximum distance of our cameras to the nearest road) and harvested brushturkeys everywhere. It could be that brushturkey occurrence would be more strongly related to the distance to larger cities such as Jayapura and Manokwari. Brushturkeys in our study sites are known to be occasionally snared, but in general, wildlife hunting in these areas tends to focus on larger animals such as pigs, rusa deer (Rusa timorensis), and cassowaries (Casuarius spp.) (Pangau-Adam and Noske 2010). Brushturkeys may simply be too small (mean weight ¼ 1,5 kg) for hunters to target in areas where larger game remains extant. In our study sites,
brushturkeys and their eggs were mostly consumed within hunters’ families and only rarely traded in markets. Our results suggest that low-level hunting and egg harvesting might not necessarily be detrimental to brushturkeys. Where brushturkeys are more heavily harvested, such as in certain parts of Papua New Guinea, local extinctions have occurred (Sinclair 2007). Further study is needed to assess the sustainability of brushturkey harvesting by local people across New Guinea, particularly with regards to traditional ecological knowledge about wildlife hunting. Habitat disturbance, particularly logging, is considered a primary threat to brushturkeys. Removing large trees may reduce the density of vegetation and the availability of plant materials for nest mound construction. As mounds tend to be associated with large trees and are frequently built in less-disturbed habitats (Jones 1988, Sinclair 2002), these birds have been predicted to avoid logged areas. Surprisingly, in our study sites, we did not find any impact of logging on the occurrence of brushturkeys. The logging intensity in both sites may have just been too low to see such an effect, whereas higher intensity logging could have had more impact. The local timber harvesting in the Arfak Mountains is mainly to supply wood for housing in the villages nearby, whereas in Nimbokrang smallscale logging is mainly to extract commercially valuable merbau trees. These logging activities may allow large trees to remain in the forest, providing suitable conditions for building nest mounds and protecting them from desiccation. The other potential threat to brushturkeys in our study sites are introduced pigs. Megapodes and their eggs are known to be preyed upon by pigs in New Guinea, Sulawesi, and the Mollucan islands (Kisokau 1976, MacKinnon 1981, Heij 2001). Because pigs are widespread throughout New Guinea, they could have a damaging effect on brushturkey persistence. However, our results suggest that pigs do not have an effect on brushturkey occurrence in either study site. It might be pigs divert a lot of the hunting pressure (i.e. people would rather hunt pigs than brushturkeys) and so could even be indirectly beneficial to brushturkeys. Pigs are the most preferred game species by humans in our study areas because of their large amount of meat. Pigs are also occasionally hunted in large numbers by clan groups so as to provide sufficient meat for community festivals and religious ceremonies (Pangau-Adam et al 2012), and this may help control pig abundance to the advantage of ground-dwelling birds. Another study in the same areas indicated that introduced pigs do not appear to compete strongly with two species of cassowary birds (Brodie and Pangau-Adam 2015). Finally, it is possible that both sites still provide sufficient alternative food resources for pigs, such that they do not prey heavily on brushturkeys. We did not detect an effect of any of the three major presumed threats on the occurrence of two brushturkey species in Papua. It is certainly plausible that, because of small sample sizes, we lacked
Table 1. Akaike Information Criteria (AIC) and parameter coefficients (SE) for null models (with the most parsimonious detection covariate but no occupancy covariates) and the final models from backward-selection stepwise model selection analysis. Model
AIC
Red-legged brushturkey Null 138.43 Stepwise 139.99 Wattled brushturkey Null 203.69 Stepwise 206.85 Species pooled Null 339.73 Stepwise 341.60
Detection
Occupancy
Logged
Elevation
Logged
Distance
Pig
0.64 (0.60) 0.81 (0.54)
na 23.39 (29.79)
na 27.58 (35.01)
na -4.24 (4.77)
na 8.52 (8.69)
0.58 (0.47) 1.03 (0.45)
na na
na na
na 25.40 (43.50)
na na
na na
na na
na na
na 0.15 (0.42)
na na
na ¼ not available.
Please cite this article as: Pangau-Adam MZ, Brodie JF, Threats to the populations of two endemic brushturkey species in Indonesian New Guinea, Journal of Asia-Pacific Biodiversity, https://doi.org/10.1016/j.japb.2019.07.005
MZ Pangau-Adam, JF Brodie / Journal of Asia-Pacific Biodiversity xxx (xxxx) xxx
the statistical power to detect effects. We note that using the exact same camera trap data set, we detected strong effects of human activities on cassowary occurrence rates; however, we obtained more detections of cassowaries during that time than we did of either brushturkey species. Local people have reported the declines in the numbers of brushturkeys (Sinclair 2007). Furthermore, even though the megapodes on mainland New Guinea are classified as “Lower Risk” (Dekker et al 2000), they are now facing habitat loss and increasing hunting pressure from expanding human populations (Sinclair 2000). Concurrent pressures from two or more threats may adversely affect the distribution and population of brushturkeys. Several megapodes that are subject to exploitation may also be affected by other pressures such as forestry or agriculture (Dekker et al 2000). It should also be noted that the occurrence of brushturkeys (i.e. whether or not a brushturkey occurred at a given camera station) is a fairly crude metric, and future studies that assess brushturkey abundance would be useful. Conflicts of interest There is no conflict of interest. Funding This study was undertaken with financial support from the Dorothea Schlözer Fellowship Program of the University of Göttingen, Germany, the Natural Sciences and Engineering Research Council of Canada, and the Canadian Foundation for Innovation. None of our funders had any influence on the content of the submitted or published manuscript, and none of them required approval of the final manuscript to be published. Acknowledgments The authors thank the Papuan Government and local communities for permission to conduct this work. They are grateful to Dance Kencim, Augustinus, and Zeth Wonggor for the assistance with field work. Appendix A. Supplementary data Supplementary data to this article can be found online at https://doi.org/10.1016/j.japb.2019.07.005. References Argeloo M, Dekker RWRJ. 1996. Exploitation of megapode eggs in Indonesia: The role off traditional methods in the conservation of megapodes. Oryx 30 (1):59e 64. Baker GC, Butchart SHM. 2000. Threats to the Maleo Macrocephalon maleo and recommendations for its conservation. Oryx 34:255e262. Benitez-Lopez A, Alkemade R, Schipper AM, et al. 2017. The impact of hunting on tropical mammal and bird populations. Science 356:180e183. BirdLife International. 2012. Aepypodius arfakianus. In: The IUCN Red List of Threatened Species 2012. Available at: https://doi.org/10.2305/IUCN.UK.2012- 1. RLTS.T22678555A40071342.en. (Accessed 9 May 2018).
5
BirdLife International. 2016. Talegalla jobiensis. In: The IUCN Red List of Threatened Species, 2016. Available at: https://doi.org/10.2305/IUCN.UK.2016- 3.RLTS. T22678572A92779263.en. (Accessed 9 May 2018). Brodie JF, Pangau-Adam M. 2015. Human impacts on two endemic cassowary species in Indonesian New Guinea. Oryx 51:354e360. Brodie JF, Giordano AJ, Dickson BG, et al. 2014. Evaluating multispecies landscape connectivity in a threatened tropical mammal community. Conservation Biology 29:122e132. Brook BW, Sodhi NS, Bradshaw CJA. 2008. Synergies among extinction drivers under global change. Trends in Ecology & Evolution 23 (8):453e460. Corlett RT. 2009. The ecology of tropical East Asia. Oxford: Oxford University Press. Corlett RT, Primack RB. 2011. Tropical Rain Forests: An Ecological and Biogeographical Comparison. Chichester, UK: Wiley and Sons. Dekker RWRJ, Wattle J. 1987. Egg and image: new and traditional uses for the Maleo (Macrocephalon maleo). In: Diamond AW, Filion FL, editors. The value of birds, vol. 6. International Council for Bird Preservation, Technical Publication No.. pp. 83e87. Dekker RWRJ, Fuller RA, Baker GC. 2000. Megapodes: Status Survey and Conservation Action Plan 2000-2004. Gland, Switzerland: WPA/BirdLife/SSC Megapode Specialist Group. IUCN and the World Pheasant Association. Doherty TS, Dickman CR, Nimmo DG, et al. 2015. Multiple threats, or multiplying the threats? Interactions between invasive predators and other ecological disturbances. Biological Conservation 190:60e68. Flannery T. 1995. Mammals of New Guinea. Chatsworth, Australia: Reed Books. Frith HJ. 1956. Breeding habits in the family of Megapodiidae. Ibis 98:620e640. Heij CJ. 2001. The biology of the Moluccan megapode Eulipoa wallacei (Aves, Galliformes, Megapodiidae) on Haruku and other Moluccan Islands; part 3: update of data until 2001 e Deinsea, vol. 8. pp. 229e241. IUCN. 2016. The IUCN Red List of Threatened Species. URL. Available at: www. iucnredlist.org Version 2017.3. . (Accessed 9 May 2018). Jones DN. 1988. Selection of incubation sites by the Australian Brush-turkey, Alectura lathami. Ibis 130:251e260. Jones DN, Dekker RWRJ, Roselaar CS. 1995. The Megapodes (Bird Families of the World). Oxford University Press. Kemp NJ, Bunett JB. 2007. A Non-native Primate (Macaca fascicularis) in Papua: Implication for Biodiversity. In: Marshall AJ, Beehler BM, editors. The Ecology of Papua: Part Two. Singapore: Periplus Editions. pp. 1251e1275. Kisokau KM. 1976. A study in the biology of the megapodes of West New Britain. Papua New Guinea Bird Society Newsletter 121:20e23. Mack A, West P. 2005. Ten thousand tonnes of small animals: wildlife consumption in Papua New Guinea, a vital resource in need of management. Resource Management in Asia- Pacific Working Paper No. 61. Canberra: Australian National University. MacKenzie DI, Nichols JD, Royle JA, et al. 2005. Occupancy estimation and modeling. San Diego, CA: Elsevier. MacKinnon J. 1981. Methods for the conservation of Maleo birds, Macrocephalon maleo on the island of Sulawesi, Indonesia. Biological Conservation 20:183e193. Pangau-Adam M, Noske R. 2010. Wildlife hunting and bird trade in northern Papua. In: Tidemann S, Gosler A, Gosford R, editors. Ethno-ornithology: Global Studies in Indigenous Ornithology, Culture, Society and Conservation. London, UK: Earthscan. pp. 73e85. Pangau-Adam M, Noske R, Muehlenberg M. 2012. Wildmeat or bushmeat? Subsistence hunting and commercial harvesting in Papua (West New Guinea), Indonesia. Human Ecology 40:611e621. Pratt TK, Beehler BM. 2015. Birds of New Guinea. Princeton, USA: Princeton University Press. Radley PM, Davis RA, Dekker RWRJ, et al. 2018. Vulnerability of megapodes (Megapodiidae, Aves) to climate change and related threats Environmental Conservation. pp. 1e11. Steadman DW. 2006. Extinction and Biogeography of Tropical Pacific Birds. University of Chicago Press. Simard M, Pinto N, Fisher J, et al. 2011. Mapping forest canopy height globally with spaceborne lidar. Journal of Geophysical Research 116:G04021. https://doi.org/ 10.1029/2011JG001708. Sinclair JR. 2000. Management recommendations for three sympatric species of megapode in Papua New Guinea. Megapode Newsletter 14:9e14. Sinclair JR. 2002. Selection of incubation mound sites by three sympatric megapodes in Papua New Guinea. The Condor 104:395e406. Sinclair JR. 2007. Are we doing enough? A review of the conservation status of megapodes and the implemetation of their action plans. Available at: www. malleefowlvictoria.org.au/2007Forum/12.pdf. (Accessed 26 January 2018).
Please cite this article as: Pangau-Adam MZ, Brodie JF, Threats to the populations of two endemic brushturkey species in Indonesian New Guinea, Journal of Asia-Pacific Biodiversity, https://doi.org/10.1016/j.japb.2019.07.005
Contents lists available at ScienceDirect
Journal of Asia-Pacific Biodiversity journal homepage: http://www.elsevier.com/locate/japb
Original Article
Threats to the populations of two endemic brushturkey species in Indonesian New Guinea Margaretha Z. Pangau-Adam a, *, Jedediah F. Brodie b a b
Department of Conservation Biology, Institute of Zoology and Anthropology, University of Göttingen, 37073, Göttingen, Germany Division of Biological Sciences & Wildlife Biology Program, University of Montana, Missoula, MT, 59812, United States
a r t i c l e i n f o
a b s t r a c t
Article history: Received 19 November 2018 Received in revised form 30 April 2019 Accepted 13 July 2019 Available online xxx
Half of megapode bird species occur in New Guinea and adjacent islands, and almost all of the species are endemic to this region. Despite rapid regional development and deforestation in New Guinea, little is known about the population ecology of these birds, many of which are threatened or endangered. We used camera traps to assess impacts of anthropogenic disturbance and introduced predators on the occurrence and local abundance of red-legged brushturkey Talegalla jobiensis in lowland forests of Nimbokrang, Papua, and the wattled brushturkey Aepypodius arfakianus in the Arfak mountains, West Papua, Indonesia. In hierarchical occupancy models, detection rates were higher in logged forest for both brushturkey species. Occurrence rates of brushturkeys were not affected by logging, hunting pressure, or pig abundance. However, as degradation of megapode habitat is increasing across New Guinea, it is predicted that concurrent pressures from two or more of these threats could affect the distribution and populations of brushturkeys. Ó 2019 National Science Museum of Korea (NSMK) and Korea National Arboretum (KNA), Publishing Services by Elsevier. This is an open access article under the CC BY-NC-ND license (http:// creativecommons.org/licenses/by-nc-nd/4.0/).
Keywords: Endemic birds Hunting Logging Megapodes Papua
Introduction The family of megapode birds (Megapodiidae) is confined to the Indo-Pacific and distributed mainly in New Guinea, where 11 of the 22 species occur (Pratt and Beehler 2015). These birds have a highly unique breeding biology, where they incubate their eggs using heat from environment sources (solar energy, volcanic activity, and microbial decomposition) and where the chicks are entirely independent after hatching (Frith 1956, Jones et al 1995). In New Guinea, megapodes bury their eggs in large mounds that they build of compost, which generate heat for egg incubation from decaying organic materials (Jones et al 1995, Sinclair 2007). Many megapodes are threatened with extinction. Over half of the species that once existed in Oceania are now extinct (Steadman 2006), and almost half of the remaining species are classified by the IUCN as threatened and exhibiting population decline (Sinclair 2007) because of habitat destruction, hunting, collection of eggs,
* Corresponding author. Biology Department, Faculty of Natural Sciences and Mathematics, Cenderawasih University, Jayapura Papua, Indonesia. E-mail addresses: [email protected] (M.Z. Pangau-Adam), jedediah.brodie@ gmail.com (J.F. Brodie). Peer review under responsibility of National Science Museum of Korea (NSMK) and Korea National Arboretum (KNA).
and introduced predators (Dekker et al 2000, IUCN 2016). A recent study reported that because of their unique ecological traits, megapodes may also be vulnerable to climate change (Radley et al 2018), possibly exacerbated by other anthropogenic threats (Brook et al 2008). In spite of the high number of megapode species occurring in New Guinea and adjacent islands, there is a lack of data on the distribution and status of megapodes there. We studied a population of red-legged brushturkey Talegalla jobiensis in lowland forests and a population of wattled brushturkey Aepypodius arfakianus in submontane forests of Papua, Indonesia, using motion-triggered camera traps. Both species are endemic to New Guinea and adjacent islands and sympatric in lower montane forests (Pratt and Beehler 2015). Wattled brushturkey inhabit the upland interior forests of the mountains of New Guinea, and red-legged brushturkey are in lowland to mid-montane forests of northern New Guinea. These brushturkeys are among the least studied and poorly known megapodes, especially with respect to their population ecology. Although both of the brushturkey species have wide distributions and they were recently classified as Least Concern on the IUCN Red List (BirdLife International 2012, 2016), increasing deforestation and habitat loss may considerably threaten their populations. Rapid regional development and growing human
https://doi.org/10.1016/j.japb.2019.07.005 pISSN2287-884X eISSN2287-9544/Ó 2019 National Science Museum of Korea (NSMK) and Korea National Arboretum (KNA), Publishing Services by Elsevier. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Please cite this article as: Pangau-Adam MZ, Brodie JF, Threats to the populations of two endemic brushturkey species in Indonesian New Guinea, Journal of Asia-Pacific Biodiversity, https://doi.org/10.1016/j.japb.2019.07.005
2
MZ Pangau-Adam, JF Brodie / Journal of Asia-Pacific Biodiversity xxx (xxxx) xxx
populations in Papua have driven the conversion of large forest areas to agricultural lands, settlements, and infrastructure. This is accompanied by logging activities that are increasing rapidly in the region, as concession companies have shifted their interest to New Guinea following the collapse of timber stocks in other parts of Indonesia. Habitat disturbance is considered among the major threats to brushturkeys and can lead to fragmentation of the species’ ranges (Dekker et al 2000). Even short of complete deforestation, selective logging can degrade the forest, reducing the quality of habitat for brushturkeys that need leaf litter for their nest mounds. Bird capture and harvesting of eggs are also serious threats to brushturkeys and other megapodes. Because their nest mounds are large and conspicuous, these are easily found by humans and other predators (Sinclair 2007). Many megapode species including brushturkeys spend long periods of time at their incubation sites (Jones et al 1995); therefore, snaring and hunting of adult birds are widespread in New Guinea (Mack and West 2005, Pangau-Adam and Noske 2010). Because brushturkeys lay substantial clutches of eggs that are large and have a high yolk content (Dekker and Wattle 1987), egg collecting is a useful expenditure of time and energy for their predators, including humans (Sinclair 2007). Unsustainable egg harvesting has led to the abandonment of nesting fields and local extinctions of some megapodes in Indonesia (Argeloo and Dekker 1996, Baker and Butchart 2000, Dekker et al 2000). Although hunting of wildlife in Papua is not prohibited, the Indonesian government has ratified laws for the protection of a number of wildlife species (Government of Indonesia Regulation No. 7 1999), and megapodes are among the protected birds. However, illegal hunting and egg collecting are still widespread (PangauAdam pers. observation). Another potential threat to brushturkeys is introduced predators. Mammal introductions in New Guinea are of conservation concern because the region lacks many placental mammal lineages. Invasive species may become an added stressor with multiple other threats such as habitat change (Doherty et al 2015). Invasive primates near Jayapura, Papua, for example, mainly inhabit fragmented forests (Kemp & Burnett 2007), and they could have significant effects on native birds that are not adapted to these nest predators (Corlett and Primack 2011), especially on forest birds facing habitat changes. There were no ungulates in New Guinea before the introduction of pigs (Sus scrofa S. celebensis) by humans thousands of years ago (Flannery 1995). Pigs are known predators on both adult megapodes and their eggs (MacKinnon 1981). As they breed quickly and are omnivorous, pigs may also affect the population and persistence of brushturkeys in New Guinea. The aim of this study was to determine whether the occurrence rates of two brushturkey species were affected by logging, hunting, and introduced pigs, while accounting for natural variation in occurrence driven by elevation and forest structure. Material and methods Study areas Fieldwork was conducted at two humid tropical forest areas, (1) in the lowlands near Nimbokrang, Papua Province and (2) in the Arfak Mountains, West Papua Province (Figure 1). The Nimbokrang lowlands comprise a mosaic of forest habitats including large portions of intact forest. The site has flat alluvial forest, much of which was flooded to a depth of a few centimeters at the time of survey. Typical canopy tree genera are Instia, Pometia, Ficus, Canarium, Alstonia, and Terminalia, while understory trees include Myristica, Syzygium, Garcinia, Diospyros, Pandanus, and palms. Large areas of
the forest are claimed as traditional or clan forest by the local people, with several different land use systems such as shifting cultivation and forest gardens. The forests have not been commercially logged, although illegal selective logging of merbau Intsia bijuga (Fabaceae) is widespread. The Arfak Mountains are one of the protected areas in West Papua, located about 35 km from the capital city of the Province, Manokwari. The topography is steep and the forests have a lower canopy than in Nimbokrang and denser understorey vegetation. There has been no commercial logging, and forest clearance for small-scale subsistence agriculture and for house construction are limited to areas near villages. The wattled brushturkey is the only megapode that inhabits this area. Field sampling In June 2014, 20 camera trap stations were set out at each study site. Reconyx HC500 camera-traps (Reconyx, Inc. Holmen, USA) were installed along transects radiating from two villages in each site. The sampling area in Nimbokrang was at 15e660 m elevation in lowland alluvial forest, and in the Arfak Mountains was at 1,030e 2,280 m elevation in lower montane forests (Flannery 1995). Cameras were deployed c. 1 km apart along each transect, usually on small game trails, stream beds, ridge tops, or in other areas that animals might use for movement or foraging. The distance from the cameras to human habitation or roads was 0.2-6 km, with various distance categories approximately equally represented. Cameras were attached to the bases of trees and housed within protective metal cases. They operated 24 hours per day, recording colour images during the day and black-and-white at night. When triggered by motion in front of the receptor, the camera recorded a sequence of three images and then did not record again for at least 30 s. All cameras in both sites were retrieved 5e7 months later. Data analysis We used hierarchical occupancy models (MacKenzie et al. 2005) to assess the response of brushturkeys to human disturbance in the form of logging, hunting, and introduced invasive pigs. These models are widely used to analyze data from camera traps and allow the robust estimation of occupancy probabilities while accounting for imperfect detection. Specifically, occupancy models partition variance in the data between an occupancy function and a detectability function, with covariates potentially applied to both. We used 5-day sampling intervals at each camera stationdas in other studies (e.g. Brodie et al 2014). This served to reduce the number of zeroes (i.e. sampling intervals without any detections) in the data; data sets with excessive numbers of zeroes, a common problem when surveying rare and elusive rainforest animals, can be problematic for model convergence and parameter estimation. To assess the study objective, we ran occupancy models with covariates for logging, hunting, and relative pig abundance. The logging term (logged) was binary, indicating whether or not the forest around the camera station had been selectively logged. As a proxy for hunting pressure, we used a Geographic Information System to measure the distance from each camera station to the nearest road or town (distance). This metric has been demonstrated to strongly predict vertebrate diversity and biomass across tropical systems (Benitez-Lopez et al 2017). As a metric of pig relative abundance (pig) at each camera station, we used the number of photographic captures of pigs per 100 trap days. Because brushturkey occupancy could also be affected by natural variation in the ecosystem, we included additional covariates that served as proxies for forest structure and abiotic conditions
Please cite this article as: Pangau-Adam MZ, Brodie JF, Threats to the populations of two endemic brushturkey species in Indonesian New Guinea, Journal of Asia-Pacific Biodiversity, https://doi.org/10.1016/j.japb.2019.07.005
MZ Pangau-Adam, JF Brodie / Journal of Asia-Pacific Biodiversity xxx (xxxx) xxx
3
Figure 1. The study sites in the Arfak Mountains (West Papua Province) and Nimbokrang (Papua Province) in Indonesian New Guinea.
(e.g. temperature), namely elevation and forest height. Elevation is the strongest determinant of forest structure, tree species composition, and temperature in this region (Corlett 2009). We measured elevation in the field using a Garmin 64S Global Positioning System unit with an internal barometric altimeter. Forest height was taken from a global map of tropical forest canopies (Simard et al 2011). We considered three detection covariates. First, we assessed whether detection varied between logged and unlogged forest, as logging can induce changes in understory structure that might affect camera visibility or animal movement behaviors. Second, we included the number of days since camera deployment (time) as a sampling covariate, as animals might avoid or be attracted to camera stations initially based on recent human presence (Brodie et al 2014). Finally, we included the total number of hours that each camera was deployed for at each station (camhours)dthis was 120 h (24 h d-1 5 d) for most sampling intervals but usually less for the last interval. Because of the number of covariates that we wished to examine, we could not assess all possible combinations of factors, partly because the model set would have been extremely large and also because, with our relatively sparse data, highly parameterized models did not converge. So we used a sequential process of selecting models. First, we chose the best detection variable by examining four models, one for each detection covariate plus an intercept-only model. Each of these four models included all of the occupancy variables. We chose the variable in the model with the lowest Akaike Information Criterion (AIC) as the detection covariate. Next, we used a backwards-selection stepwise procedure to
identify the most parsimonious occupancy covariates. We started with a global model that included the detection covariate and all of the occupancy covariates and sequentially removed occupancy variables with the lowest absolute value z-statistics until the AIC was minimized. Finally, we compared this top model to a null model with the detection covariate but only a model intercept in the occupancy function. We used model averaging between the most parsimonious model and the null model for multimodel inference. We assessed multicollinearity among predictor variables before model analysis and did not include variables with jrj > 0.7 in the same model. We analyzed the two brushturkey species separately and also by pooling their data to determine general patterns that affected both (while also increasing the sample size and thus statistical power). For the combined-species analysis, we did not include elevation or forest height covariates as these differed so greatly between the study areas. Results Several camera traps at each location were stolen. Out of a total of 2211 sampling days across 16 camera stations in the Arfak Mountains and 2433 sampling days across 12 stations in Nimbokrang, we obtained 31 detections of wattled brushturkeys and 19 detections of red-legged brushturkeys. For the red-legged brushturkey, logged was the best detection covariate, with detection rate being higher in logged forest. After stepwise variable selection, the most parsimonious model included
Please cite this article as: Pangau-Adam MZ, Brodie JF, Threats to the populations of two endemic brushturkey species in Indonesian New Guinea, Journal of Asia-Pacific Biodiversity, https://doi.org/10.1016/j.japb.2019.07.005
4
MZ Pangau-Adam, JF Brodie / Journal of Asia-Pacific Biodiversity xxx (xxxx) xxx
positive effects of elevation, logging, and pig relative abundance, and a negative effect of distance to the nearest road or village, on brushturkey occupancy. For all of the occupancy variables, the standard error (SE) exceeded the parameter coefficient in magnitude, indicative of a very weak (at best) effect. Moreover, the top model was w1.5 AIC units worse than the intercept-only model (Table 1). For the wattled brushturkey, logged was the best detection covariate, with detection rate being higher in logged forest. Forest height and elevation were correlated (r ¼ 0.73), and so only the latter was included in subsequent models, as it had a much greater range of variation than the former. The most parsimonious occupancy model included a positive effect of distance to the nearest road or village on occupancy, but the SE was larger than the coefficient, and the model was w3 AIC units worse than the interceptonly model (Table 1). For the two species combined, no detection covariate outperformed the intercept-only detection model. The most parsimonious occupancy model included a positive effect of distance to the nearest road or village on occupancy, but the SE was larger than the coefficient, and the model was w2 AIC units worse than the intercept-only model (Table 1). Based on the best-performing, intercept-only detection models, the average proportion of each study area occupied by brushturkeys (i.e. the model intercept) was 0.21 (SE ¼ 0.66) for red-legged brushturkeys in Nimbokrang and 0.70 (0.60) for wattled brushturkeys in the Arfak Mountains. Discussion This is the first assessment on the population ecology and factors influencing occurrence of the red-legged brushturkey and the wattled brushturkey in Indonesian New Guinea. Although hunting and egg harvesting are common threats to megapodes (Jones et al 1995, Dekker et al 2000), we did not detect an effect of potential hunting pressure (distance to roads and villages) on occurrence rates of brushturkey. It may be that the roads and towns in the study areas were too small, or the human density too low, to see these effects, or that hunters simply ranged very widely (>6 km, the maximum distance of our cameras to the nearest road) and harvested brushturkeys everywhere. It could be that brushturkey occurrence would be more strongly related to the distance to larger cities such as Jayapura and Manokwari. Brushturkeys in our study sites are known to be occasionally snared, but in general, wildlife hunting in these areas tends to focus on larger animals such as pigs, rusa deer (Rusa timorensis), and cassowaries (Casuarius spp.) (Pangau-Adam and Noske 2010). Brushturkeys may simply be too small (mean weight ¼ 1,5 kg) for hunters to target in areas where larger game remains extant. In our study sites,
brushturkeys and their eggs were mostly consumed within hunters’ families and only rarely traded in markets. Our results suggest that low-level hunting and egg harvesting might not necessarily be detrimental to brushturkeys. Where brushturkeys are more heavily harvested, such as in certain parts of Papua New Guinea, local extinctions have occurred (Sinclair 2007). Further study is needed to assess the sustainability of brushturkey harvesting by local people across New Guinea, particularly with regards to traditional ecological knowledge about wildlife hunting. Habitat disturbance, particularly logging, is considered a primary threat to brushturkeys. Removing large trees may reduce the density of vegetation and the availability of plant materials for nest mound construction. As mounds tend to be associated with large trees and are frequently built in less-disturbed habitats (Jones 1988, Sinclair 2002), these birds have been predicted to avoid logged areas. Surprisingly, in our study sites, we did not find any impact of logging on the occurrence of brushturkeys. The logging intensity in both sites may have just been too low to see such an effect, whereas higher intensity logging could have had more impact. The local timber harvesting in the Arfak Mountains is mainly to supply wood for housing in the villages nearby, whereas in Nimbokrang smallscale logging is mainly to extract commercially valuable merbau trees. These logging activities may allow large trees to remain in the forest, providing suitable conditions for building nest mounds and protecting them from desiccation. The other potential threat to brushturkeys in our study sites are introduced pigs. Megapodes and their eggs are known to be preyed upon by pigs in New Guinea, Sulawesi, and the Mollucan islands (Kisokau 1976, MacKinnon 1981, Heij 2001). Because pigs are widespread throughout New Guinea, they could have a damaging effect on brushturkey persistence. However, our results suggest that pigs do not have an effect on brushturkey occurrence in either study site. It might be pigs divert a lot of the hunting pressure (i.e. people would rather hunt pigs than brushturkeys) and so could even be indirectly beneficial to brushturkeys. Pigs are the most preferred game species by humans in our study areas because of their large amount of meat. Pigs are also occasionally hunted in large numbers by clan groups so as to provide sufficient meat for community festivals and religious ceremonies (Pangau-Adam et al 2012), and this may help control pig abundance to the advantage of ground-dwelling birds. Another study in the same areas indicated that introduced pigs do not appear to compete strongly with two species of cassowary birds (Brodie and Pangau-Adam 2015). Finally, it is possible that both sites still provide sufficient alternative food resources for pigs, such that they do not prey heavily on brushturkeys. We did not detect an effect of any of the three major presumed threats on the occurrence of two brushturkey species in Papua. It is certainly plausible that, because of small sample sizes, we lacked
Table 1. Akaike Information Criteria (AIC) and parameter coefficients (SE) for null models (with the most parsimonious detection covariate but no occupancy covariates) and the final models from backward-selection stepwise model selection analysis. Model
AIC
Red-legged brushturkey Null 138.43 Stepwise 139.99 Wattled brushturkey Null 203.69 Stepwise 206.85 Species pooled Null 339.73 Stepwise 341.60
Detection
Occupancy
Logged
Elevation
Logged
Distance
Pig
0.64 (0.60) 0.81 (0.54)
na 23.39 (29.79)
na 27.58 (35.01)
na -4.24 (4.77)
na 8.52 (8.69)
0.58 (0.47) 1.03 (0.45)
na na
na na
na 25.40 (43.50)
na na
na na
na na
na na
na 0.15 (0.42)
na na
na ¼ not available.
Please cite this article as: Pangau-Adam MZ, Brodie JF, Threats to the populations of two endemic brushturkey species in Indonesian New Guinea, Journal of Asia-Pacific Biodiversity, https://doi.org/10.1016/j.japb.2019.07.005
MZ Pangau-Adam, JF Brodie / Journal of Asia-Pacific Biodiversity xxx (xxxx) xxx
the statistical power to detect effects. We note that using the exact same camera trap data set, we detected strong effects of human activities on cassowary occurrence rates; however, we obtained more detections of cassowaries during that time than we did of either brushturkey species. Local people have reported the declines in the numbers of brushturkeys (Sinclair 2007). Furthermore, even though the megapodes on mainland New Guinea are classified as “Lower Risk” (Dekker et al 2000), they are now facing habitat loss and increasing hunting pressure from expanding human populations (Sinclair 2000). Concurrent pressures from two or more threats may adversely affect the distribution and population of brushturkeys. Several megapodes that are subject to exploitation may also be affected by other pressures such as forestry or agriculture (Dekker et al 2000). It should also be noted that the occurrence of brushturkeys (i.e. whether or not a brushturkey occurred at a given camera station) is a fairly crude metric, and future studies that assess brushturkey abundance would be useful. Conflicts of interest There is no conflict of interest. Funding This study was undertaken with financial support from the Dorothea Schlözer Fellowship Program of the University of Göttingen, Germany, the Natural Sciences and Engineering Research Council of Canada, and the Canadian Foundation for Innovation. None of our funders had any influence on the content of the submitted or published manuscript, and none of them required approval of the final manuscript to be published. Acknowledgments The authors thank the Papuan Government and local communities for permission to conduct this work. They are grateful to Dance Kencim, Augustinus, and Zeth Wonggor for the assistance with field work. Appendix A. Supplementary data Supplementary data to this article can be found online at https://doi.org/10.1016/j.japb.2019.07.005. References Argeloo M, Dekker RWRJ. 1996. Exploitation of megapode eggs in Indonesia: The role off traditional methods in the conservation of megapodes. Oryx 30 (1):59e 64. Baker GC, Butchart SHM. 2000. Threats to the Maleo Macrocephalon maleo and recommendations for its conservation. Oryx 34:255e262. Benitez-Lopez A, Alkemade R, Schipper AM, et al. 2017. The impact of hunting on tropical mammal and bird populations. Science 356:180e183. BirdLife International. 2012. Aepypodius arfakianus. In: The IUCN Red List of Threatened Species 2012. Available at: https://doi.org/10.2305/IUCN.UK.2012- 1. RLTS.T22678555A40071342.en. (Accessed 9 May 2018).
5
BirdLife International. 2016. Talegalla jobiensis. In: The IUCN Red List of Threatened Species, 2016. Available at: https://doi.org/10.2305/IUCN.UK.2016- 3.RLTS. T22678572A92779263.en. (Accessed 9 May 2018). Brodie JF, Pangau-Adam M. 2015. Human impacts on two endemic cassowary species in Indonesian New Guinea. Oryx 51:354e360. Brodie JF, Giordano AJ, Dickson BG, et al. 2014. Evaluating multispecies landscape connectivity in a threatened tropical mammal community. Conservation Biology 29:122e132. Brook BW, Sodhi NS, Bradshaw CJA. 2008. Synergies among extinction drivers under global change. Trends in Ecology & Evolution 23 (8):453e460. Corlett RT. 2009. The ecology of tropical East Asia. Oxford: Oxford University Press. Corlett RT, Primack RB. 2011. Tropical Rain Forests: An Ecological and Biogeographical Comparison. Chichester, UK: Wiley and Sons. Dekker RWRJ, Wattle J. 1987. Egg and image: new and traditional uses for the Maleo (Macrocephalon maleo). In: Diamond AW, Filion FL, editors. The value of birds, vol. 6. International Council for Bird Preservation, Technical Publication No.. pp. 83e87. Dekker RWRJ, Fuller RA, Baker GC. 2000. Megapodes: Status Survey and Conservation Action Plan 2000-2004. Gland, Switzerland: WPA/BirdLife/SSC Megapode Specialist Group. IUCN and the World Pheasant Association. Doherty TS, Dickman CR, Nimmo DG, et al. 2015. Multiple threats, or multiplying the threats? Interactions between invasive predators and other ecological disturbances. Biological Conservation 190:60e68. Flannery T. 1995. Mammals of New Guinea. Chatsworth, Australia: Reed Books. Frith HJ. 1956. Breeding habits in the family of Megapodiidae. Ibis 98:620e640. Heij CJ. 2001. The biology of the Moluccan megapode Eulipoa wallacei (Aves, Galliformes, Megapodiidae) on Haruku and other Moluccan Islands; part 3: update of data until 2001 e Deinsea, vol. 8. pp. 229e241. IUCN. 2016. The IUCN Red List of Threatened Species. URL. Available at: www. iucnredlist.org Version 2017.3. . (Accessed 9 May 2018). Jones DN. 1988. Selection of incubation sites by the Australian Brush-turkey, Alectura lathami. Ibis 130:251e260. Jones DN, Dekker RWRJ, Roselaar CS. 1995. The Megapodes (Bird Families of the World). Oxford University Press. Kemp NJ, Bunett JB. 2007. A Non-native Primate (Macaca fascicularis) in Papua: Implication for Biodiversity. In: Marshall AJ, Beehler BM, editors. The Ecology of Papua: Part Two. Singapore: Periplus Editions. pp. 1251e1275. Kisokau KM. 1976. A study in the biology of the megapodes of West New Britain. Papua New Guinea Bird Society Newsletter 121:20e23. Mack A, West P. 2005. Ten thousand tonnes of small animals: wildlife consumption in Papua New Guinea, a vital resource in need of management. Resource Management in Asia- Pacific Working Paper No. 61. Canberra: Australian National University. MacKenzie DI, Nichols JD, Royle JA, et al. 2005. Occupancy estimation and modeling. San Diego, CA: Elsevier. MacKinnon J. 1981. Methods for the conservation of Maleo birds, Macrocephalon maleo on the island of Sulawesi, Indonesia. Biological Conservation 20:183e193. Pangau-Adam M, Noske R. 2010. Wildlife hunting and bird trade in northern Papua. In: Tidemann S, Gosler A, Gosford R, editors. Ethno-ornithology: Global Studies in Indigenous Ornithology, Culture, Society and Conservation. London, UK: Earthscan. pp. 73e85. Pangau-Adam M, Noske R, Muehlenberg M. 2012. Wildmeat or bushmeat? Subsistence hunting and commercial harvesting in Papua (West New Guinea), Indonesia. Human Ecology 40:611e621. Pratt TK, Beehler BM. 2015. Birds of New Guinea. Princeton, USA: Princeton University Press. Radley PM, Davis RA, Dekker RWRJ, et al. 2018. Vulnerability of megapodes (Megapodiidae, Aves) to climate change and related threats Environmental Conservation. pp. 1e11. Steadman DW. 2006. Extinction and Biogeography of Tropical Pacific Birds. University of Chicago Press. Simard M, Pinto N, Fisher J, et al. 2011. Mapping forest canopy height globally with spaceborne lidar. Journal of Geophysical Research 116:G04021. https://doi.org/ 10.1029/2011JG001708. Sinclair JR. 2000. Management recommendations for three sympatric species of megapode in Papua New Guinea. Megapode Newsletter 14:9e14. Sinclair JR. 2002. Selection of incubation mound sites by three sympatric megapodes in Papua New Guinea. The Condor 104:395e406. Sinclair JR. 2007. Are we doing enough? A review of the conservation status of megapodes and the implemetation of their action plans. Available at: www. malleefowlvictoria.org.au/2007Forum/12.pdf. (Accessed 26 January 2018).
Please cite this article as: Pangau-Adam MZ, Brodie JF, Threats to the populations of two endemic brushturkey species in Indonesian New Guinea, Journal of Asia-Pacific Biodiversity, https://doi.org/10.1016/j.japb.2019.07.005