Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Wildlife Research Wildlife Research Society
Ecology, management and conservation in natural and modified habitats
RESEARCH ARTICLE

Human influence on burrow activity of the Chinese pangolin in Nepal

Ambika P. Khatiwada https://orcid.org/0000-0002-4000-8301 A B C D * , Wendy Wright https://orcid.org/0000-0003-3388-1273 E , Kyran Kunkel F , Monsoon P. Khatiwada A D , Carly Waterman C G , Santosh Bhattarai H , Hem S. Baral I , Chiranjibi P. Pokheral B and Fredrik Dalerum A J K
+ Author Affiliations
- Author Affiliations

A Biodiversity Research Institute (University of Oviedo, Principado of Asturias, Spanish National Research Council), Mieres Campus, University of Oviedo, 33600 Mieres, Asturias, Spain.

B National Trust for Nature Conservation, Khumaltar, Lalitpur 44700, Nepal.

C IUCN SSC Pangolin Specialist Group, Zoological Society of London, Regent’s Park, NW1 4RY, UK.

D Society for Conservation Biology – Nepal Chapter, Bagdol, Lalitpur 44700, Nepal.

E Future Regions Research Centre, Federation University Australia, Gippsland Campus, Churchill, Vic. 3842, Australia.

F Conservation Science Collaborative, Bozeman, MT 59715, USA.

G Conservation and policy, Zoological Society of London, Regent’s Park, London NW1 4RY, England.

H Nepal Conservation and Research Center, Ratnanagar-08, Chitwan 44204, Nepal.

I Zoological Society of London, Nepal office, Bishal Nagar Marg, Kathmandu 44600, Nepal.

J Department of Zoology, Stockholm University, 10691 Stockholm, Sweden.

K Mammal Research Institute, Department of Zoology and Entomology, University of Pretoria, 0028 Pretoria, South Africa.

* Correspondence to: ambika.pd.khatiwada@gmail.com

Handling Editor: Weihong Ji

Wildlife Research 50(1) 76-83 https://doi.org/10.1071/WR21024
Submitted: 24 January 2021  Accepted: 21 May 2022   Published: 25 July 2022

© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Context: People and wildlife are coming into greater contact worldwide because of the increasing human footprint. Although some species tolerate certain levels of human activities, others are vulnerable to human disturbance, potentially altering their spatial or temporal patterns of activity in response to disturbance by humans.

Aims: We evaluated the influence of human activity on burrow activity of the Chinese pangolin, a Critically Endangered species that is heavily persecuted for subsistence and illegal trade.

Methods: We deployed remotely triggered camera traps at pangolin burrows located at four sites with contrasting levels of human density and infrastructure in Nepal, and estimated burrow-activity patterns of pangolins by using a kernel-density estimator based on the time stamp of camera trap observations.

Key results: Our findings did not suggest that anthropogenic disturbance affected pangolin burrow activity, but we acknowledge that these findings were based on a limited number of observations. Peak pangolin burrow activity was observed after midnight in three of the study sites, including those with highest and lowest levels of human activity. The fourth area, which had intermediate levels of human activity, had an earlier peak in burrow activity, possibly caused by prey deficiency owing to intense agriculture.

Conclusions: We suggest that pangolins may tolerate human activity because of their strictly nocturnal temporal niche, but that this tolerance has made them vulnerable to poaching because it allows them to co-exist spatially with humans.

Implications: Nocturnal species may be particularly prone to non-conflict-related persecution, because they may be easily accessible targets for illegal hunting activities.

Keywords: Asia, conservation, human disturbance, mammal, Manis pentadactyla, Nepal, persecution, temporal niche.


References

Acharya, KP, Paudel, PK, Neupane, PR, and Köhl, M (2016). Human-wildlife conflicts in Nepal: patterns of human fatalities and injuries caused by large mammals. PLoS ONE 11, e0161717.
Human-wildlife conflicts in Nepal: patterns of human fatalities and injuries caused by large mammals.Crossref | GoogleScholarGoogle Scholar |

Baker, SE, Cain, R, Van Kesteren, F, Zommers, ZA, D’cruze, N, and Macdonald, DW (2013). Rough trade: animal welfare in the global wildlife trade. BioScience 63, 928–938.
Rough trade: animal welfare in the global wildlife trade.Crossref | GoogleScholarGoogle Scholar |

Benjamini, Y, and Hochberg, Y (1995). Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society 57, 289–300.
Controlling the false discovery rate: a practical and powerful approach to multiple testing.Crossref | GoogleScholarGoogle Scholar |

Bennie, JJ, Duffy, JP, Inger, R, and Gaston, KJ (2014). Biogeography of time partitioning in mammals. Proceedings of the National Academy of Sciences of the United States of America 111, 13727–13732.
Biogeography of time partitioning in mammals.Crossref | GoogleScholarGoogle Scholar |

Bhattarai, BR, Wright, W, and Khatiwada, AP (2016). Illegal hunting of prey species in the northern section of Bardia national park, Nepal: implications for carnivore conservation. Environments 3, 32.
Illegal hunting of prey species in the northern section of Bardia national park, Nepal: implications for carnivore conservation.Crossref | GoogleScholarGoogle Scholar |

Bhattarai, BR, Wright, W, Poudel, BS, Aryal, A, Yadav, BP, and Wagle, R (2017). Shifting paradigms for Nepal’s protected areas: history, challenges and relationships. Journal of Mountain Science 14, 964–979.
Shifting paradigms for Nepal’s protected areas: history, challenges and relationships.Crossref | GoogleScholarGoogle Scholar |

Biggs, D, Courchamp, F, Martin, R, and Possingham, HP (2013). Legal trade of Africa’s rhino horns. Science 339, 1038–1039.
Legal trade of Africa’s rhino horns.Crossref | GoogleScholarGoogle Scholar |

Carter, NH, Shrestha, BK, Karki, JB, Pradhan, NMB, and Liu, J (2012). Coexistence between wildlife and humans at fine spatial scales. Proceedings of the National Academy of Sciences of the United States of America 109, 15360–15365.
Coexistence between wildlife and humans at fine spatial scales.Crossref | GoogleScholarGoogle Scholar |

Challender, D (2011). Asian pangolins: increasing affluence driving hunting pressure. TRAFFIC Bulletin 23, 92–93.

Challender DWS, Waterman C, Baillie JEM (2014) ‘Scaling up pangolin conservation. IUCN SSC Pangolin specialist group conservation action plan.’ (Zoological Society of London: London, UK)

Challender D, Wu S, Kaspal P, Khatiwada A, Ghose A, Ching-Min Sun N, Mohapatra RK, Laxmi Suwal T (2019) Manis pentadactyla (errata version published in 2020). The IUCN Red List of Threatened Species 2019. Available at https://www.iucnredlist.org/species/12764/168392151 [Accessed 2 January 2021]

Challender DWS, Nash HC, Waterman C (Eds) (2020) ‘Pangolins: science, society and conservation.’ (Elsevier Academic Press: London, UK)

Clinchy, M, Zanette, LY, Roberts, D, Suraci, JP, Buesching, CD, Newman, C, and Macdonald, DW (2016). Fear of the human ‘super predator’ far exceeds the fear of large carnivores in a model mesocarnivore. Behavioral Ecology 27, 1826–1832.
Fear of the human ‘super predator’ far exceeds the fear of large carnivores in a model mesocarnivore.Crossref | GoogleScholarGoogle Scholar |

Díaz-Ruiz, F, Caro, J, Delibes-Mateos, M, Arroyo, B, and Ferreras, P (2016). Drivers of red fox (Vulpes vulpes) daily activity: prey availability, human disturbance or habitat structure? Journal of Zoology 298, 128–138.
Drivers of red fox (Vulpes vulpes) daily activity: prey availability, human disturbance or habitat structure?Crossref | GoogleScholarGoogle Scholar |

Eaton, JA, Shepherd, CR, Rheindt, FE, Harris, JBC, van Balen, SB, Wilcove, DS, and Collar, NJ (2015). Trade-driven extinctions and near-extinctions of avian taxa in Sundaic Indonesia. Forktail 31, 1–12.

Frey, S, Fisher, JT, Burton, AC, and Volpe, JP (2017). Investigating animal activity patterns and temporal niche partitioning using camera-trap data: challenges and opportunities. Remote Sensing in Ecology and Conservation 3, 123–132.
Investigating animal activity patterns and temporal niche partitioning using camera-trap data: challenges and opportunities.Crossref | GoogleScholarGoogle Scholar |

Frid, A, and Dill, LM (2002). Human-caused disturbance stimuli as a form of predation risk. Conservation Ecology 6, 11.
Human-caused disturbance stimuli as a form of predation risk.Crossref | GoogleScholarGoogle Scholar |

Gaynor, KM, Hojnowski, CE, Carter, NH, and Brashares, JS (2018). The influence of human disturbance on wildlife nocturnality. Science 360, 1232–1235.
The influence of human disturbance on wildlife nocturnality.Crossref | GoogleScholarGoogle Scholar |

Gerkema, MP, Davies, WIL, Foster, RG, Menaker, M, and Hut, RA (2013). The nocturnal bottleneck and the evolution of activity patterns in mammals. Proceedings of the Royal Society B: Biological Sciences 280, 20130508.
The nocturnal bottleneck and the evolution of activity patterns in mammals.Crossref | GoogleScholarGoogle Scholar |

Gurung, JB (1996). A pangolin survey in Royal Nagarjung forest in Kathmandu, Nepal. Tiger Paper 23, 29–32.

Halle S (2000) Ecological relevance of daily activity patterns. In ‘Activity patterns in small mammals’. (Eds S Halle, NC Stenseth) pp. 67–90. (Springer: Berlin, Germany)

Heath, ME (1987). Twenty-four-hour variations in activity, core temperature, metabolic rate, and respiratory quotient in captive Chinese pangolins. Zoo Biology 6, 1–10.
Twenty-four-hour variations in activity, core temperature, metabolic rate, and respiratory quotient in captive Chinese pangolins.Crossref | GoogleScholarGoogle Scholar |

Heath, ME, and Vanderlip, SL (1988). Biology, husbandry, and veterinary care of captive Chinese pangolins (Manis pentadactyla). Zoo Biology 7, 293–312.
Biology, husbandry, and veterinary care of captive Chinese pangolins (Manis pentadactyla).Crossref | GoogleScholarGoogle Scholar |

Heinrich, S, Koehncke, A, and Shepherd, CR (2019). The role of Germany in the illegal global pangolin trade. Global Ecology and Conservation 20, e00736.
The role of Germany in the illegal global pangolin trade.Crossref | GoogleScholarGoogle Scholar |

Hertel, AG, Swenson, JE, and Bischof, R (2017). A case for considering individual variation in diel activity patterns. Behavioral Ecology 28, 1524–1531.
A case for considering individual variation in diel activity patterns.Crossref | GoogleScholarGoogle Scholar |

Ikeda, T, Uchida, K, Matsuura, Y, Takahashi, H, Yoshida, T, Kaji, K, and Koizumi, I (2016). Seasonal and diel activity patterns of eight sympatric mammals in northern Japan revealed by an intensive camera-trap survey. PLoS ONE 11, e0163602.
Seasonal and diel activity patterns of eight sympatric mammals in northern Japan revealed by an intensive camera-trap survey.Crossref | GoogleScholarGoogle Scholar |

Khatiwada AP, Wright W, Roe D, Suwal T, Thapa S, Kaspal P, Poudel K (2020) Community conservation in Nepal – opportunities and challenges for pangolin conservation. In ‘Pangolins: science, society and conservation’. (Eds DWS Challender, HC Nash, C Waterman) pp. 395–409. (Elsevier Academic Press: London, UK)

Khwaja, H, Buchan, C, Wearn, OR, Bahaa-el-din, L, Bantlin, D, Bernard, H, Bitariho, R, Bohm, T, Borah, J, Brodie, J, Chutipong, W, duPreez, B, Ebang-Mbele, A, Edwards, S, Fairet, E, Frechette, JL, Garside, A, Gibson, L, Giordano, A, Gopi, GV, Granados, A, Gubbi, S, Harich, F, Haurez, B, Havmøller, RW, Helmy, O, Isbell, LA, Jenks, K, Kalle, R, Kamjing, A, Khamcha, D, Kiebou-Opepa, C, Kinnaird, M, Kruger, C, Laudisoit, A, Lynam, A, Macdonald, SE, Mathai, J, Sienne, JM, Meier, A, Mills, D, Mohd-Azlan, J, Nakashima, Y, Nash, HC, Ngoprasert, D, Nguyen, A, O’Brien, T, Olson, D, Orbell, C, Poulsen, J, Ramesh, T, Reeder, DA, Reyna, R, Rich, LN, Rode-Margono, J, Rovero, F, Sheil, D, Shirley, MH, Stratford, K, Sukumal, N, Suwanrat, S, Tantipisanuh, N, Tilker, A, Van Berkel, T, Van der Weyde, LK, Varney, M, Weise, F, Wiesel, I, Wilting, A, Wong, ST, Waterman, C, and Challender, DWS (2019). Pangolins in global camera trap data: implications for ecological monitoring. Global Ecology and Conservation 20, e00769.
Pangolins in global camera trap data: implications for ecological monitoring.Crossref | GoogleScholarGoogle Scholar |

Lashley, MA, Cove, MV, Chitwood, MC, Penido, G, Gardner, B, DePerno, CS, and Moorman, CE (2018). Estimating wildlife activity curves: comparison of methods and sample size. Scientific Reports 8, 4173.
Estimating wildlife activity curves: comparison of methods and sample size.Crossref | GoogleScholarGoogle Scholar |

Lin JS (2011) Home range and burrow utilization in Formosan pangolin (Manis pentadactyla pentadactyla) at Luanshan, Taitung. MSc thesis, National Pingtung University of Science and Technology, Neipu Township, Taiwan.

Mugume, S, Isabirye-Basuta, G, Otali, E, Reyna-Hurtado, R, and Chapman, CA (2015). How do human activities influence the status and distribution of terrestrial mammals in forest reserves? Journal of Mammalogy 96, 998–1004.
How do human activities influence the status and distribution of terrestrial mammals in forest reserves?Crossref | GoogleScholarGoogle Scholar |

Nickel, BA, Suraci, JP, Allen, ML, and Wilmers, CC (2020). Human presence and human footprint have non-equivalent effects on wildlife spatiotemporal habitat use. Biological Conservation 241, 108383.
Human presence and human footprint have non-equivalent effects on wildlife spatiotemporal habitat use.Crossref | GoogleScholarGoogle Scholar |

O’Brien, TG, Kinnaird, MF, and Wibisono, HT (2003). Crouching tigers, hidden prey: sumatran tiger and prey populations in a tropical forest landscape. Animal Conservation 6, 131–139.
Crouching tigers, hidden prey: sumatran tiger and prey populations in a tropical forest landscape.Crossref | GoogleScholarGoogle Scholar |

Paudel, PK, Acharya, KP, Baral, HS, Heinen, JT, and Jnawali, SR (2020). Trends, patterns, and networks of illicit wildlife trade in Nepal: a national synthesis. Conservation Science and Practice 2, e247.
Trends, patterns, and networks of illicit wildlife trade in Nepal: a national synthesis.Crossref | GoogleScholarGoogle Scholar |

Ridout, MS, and Linkie, M (2009). Estimating overlap of daily activity patterns from camera trap data. Journal of Agricultural, Biological, and Environmental Statistics 14, 322–337.
Estimating overlap of daily activity patterns from camera trap data.Crossref | GoogleScholarGoogle Scholar |

Ross, J, Hearn, AJ, Johnson, PJ, and Macdonald, DW (2013). Activity patterns and temporal avoidance by prey in response to Sunda clouded leopard predation risk. Journal of Zoology 290, 96–106.
Activity patterns and temporal avoidance by prey in response to Sunda clouded leopard predation risk.Crossref | GoogleScholarGoogle Scholar |

Schmid, F, and Schmidt, A (2006). Nonparametric estimation of the coefficient of overlapping: theory and empirical application. Computational Statistics & Data Analysis 50, 1583–1596.
Nonparametric estimation of the coefficient of overlapping: theory and empirical application.Crossref | GoogleScholarGoogle Scholar |

Smith, JA, Suraci, JP, Clinchy, M, Crawford, A, Roberts, D, Zanette, LY, and Wilmers, CC (2017). Fear of the human ‘super predator’ reduces feeding time in large carnivores. Proceedings of the Royal Society B: Biological Science 284, 20170433.
Fear of the human ‘super predator’ reduces feeding time in large carnivores.Crossref | GoogleScholarGoogle Scholar |

Smith, JA, Thomas, AC, Levi, T, Wang, Y, and Wilmers, CC (2018). Human activity reduces niche partitioning among three widespread mesocarnivores. Oikos 127, 890–901.
Human activity reduces niche partitioning among three widespread mesocarnivores.Crossref | GoogleScholarGoogle Scholar |

Sun C-M, Lin J-S, Lai C-Y, Pei KJ-C (2015) Home range, density, habitat preference and modeling of the Taiwanese pangolins (Manis pentadactyla pentadactyla) in south-eastern Taiwan. In ‘First international conference on Pangolin conservation, trade and rehabilitation’. (Eds R Jansen, A Kotze, L Sibiya) p. 28. (Mabula Game Reserve: South Africa)

Suraci, JP, Clinchy, M, Zanette, LY, and Wilmers, CC (2019). Fear of humans as apex predators has landscape-scale impacts from mountain lions to mice. Ecology Letters 22, 1578–1586.
Fear of humans as apex predators has landscape-scale impacts from mountain lions to mice.Crossref | GoogleScholarGoogle Scholar |

Takahashi JS, Turek FW, Moore RY (2001) ‘Handbook of behavioral neurobiology: circadian clocks.’ (Springer: NY, USA)

Tan, WS, Hamzah, NbA, Saaban, S, Zawakhir, NA, Rao, Y, Jamaluddin, N, Cheong, F, Khalid, Nb, Saat, NIM, Ee, ENbZ, Hamdan, Ab, Chow, MM, Low, CP, Voon, M, Liang, SH, Tyson, M, and Gumal, MT (2018). Observations of occurrence and daily activity patterns of ungulates in the Endau Rompin Landscape, peninsular Malaysia. Journal of Threatened Taxa 10, 11245–11253.
Observations of occurrence and daily activity patterns of ungulates in the Endau Rompin Landscape, peninsular Malaysia.Crossref | GoogleScholarGoogle Scholar |

Underwood, FM, Burn, RW, and Milliken, T (2013). Dissecting the illegal ivory trade: an analysis of ivory seizures data. PLoS ONE 8, e76539.
Dissecting the illegal ivory trade: an analysis of ivory seizures data.Crossref | GoogleScholarGoogle Scholar |

Weyer, NM, Fuller, A, Haw, AJ, Meyer, LCR, Mitchell, D, Picker, M, Rey, B, and Hetem, RS (2020). Increased diurnal activity is indicative of energy deficit in a nocturnal mammal, the Aardvark. Frontiers in Physiology 11, 637.
Increased diurnal activity is indicative of energy deficit in a nocturnal mammal, the Aardvark.Crossref | GoogleScholarGoogle Scholar |

Williams, JB, Anderson, MD, and Richardson, PRK (1997). Seasonal differences in field metabolism, water requirements, and foraging behavior of free-living aardwolves. Ecology 78, 2588–2602.
Seasonal differences in field metabolism, water requirements, and foraging behavior of free-living aardwolves.Crossref | GoogleScholarGoogle Scholar |

Wu, S, Liu, N, Zhang, Y, and Ma, G (2004). Assessment of threatened status of Chinese pangolin (Manis pentadactyla). Chinese Journal of Applied Environmental Biology 10, 456–461.

Wu S, Sun NC-M, Zhang F, Yu Y, Ades G, Suwal TL, Jiang Z (2020) Chinese pangolin Manis pentadactyla (Linnaeus, 1758). In ‘Pangolins: science, society and conservation’. (Eds DWS Challender, HC Nash, C Waterman) pp. 49–70. (Elsevier Academic Press: London, UK)

Wyatt, T (2011). The illegal trade of raptors in the Russian Federation. Contemporary Justice Review 14, 103–123.
The illegal trade of raptors in the Russian Federation.Crossref | GoogleScholarGoogle Scholar |