Advertisement

A field and laboratory-based assessment of the distribution of large- and meso-carnivore species in the newly established Murree, Kotli Sattian, and Kahuta National Park, Pakistan

  • Rukhsana KhatoonEmail author
  • Tariq Mehmood
  • Maqsood Anwar
  • Ume Habiba
  • Lori S. Eggert
  • Matthew E. Gompper
Original Paper
  • 22 Downloads

Abstract

Recent carnivore distributions in eastern Pakistan are poorly documented. In an effort to fill knowledge gaps, we combined field and laboratory molecular approaches to identify the large- and mid-sized mammalian carnivores in Murree, Kotli Sattian, and Kahuta National Park in Rawalpindi, Punjab. A total of 23 sites, each with a transect of 1–4 km in length, were identified and visited monthly over 24 months in 2016–2018. Fecal samples (n = 317) were collected and identified to species in the field based on morphology, odor, and additional signs. A subset (n = 150) of these samples was genetically identified to species using primers designed to amplify an informative region of the canid, felid, mustelid, and viverrid mitochondrial control region. Identified carnivore species for the park include leopard, leopard cat, jungle cat, red fox, golden jackal, small Indian civet, and Canis spp. For leopard, red fox, and golden jackal, field identification rates were accurate at a true-positive rate ≥ 63%. However, there was a notably high rate of field misidentification of putative jungle cat and yellow-throated marten samples, most of which were genetically identified as leopard cat or non-Carnivora samples. We mapped fecal sample presence points based on both morphological and genetically confirmed samples. For five of six dyadic combinations of pairwise species segregation patterns, there was evidence of high rates of non-random co-occurrence of red fox and jackal (p ≤ 0.05). For the other five pairwise combinations, no statistical support was found for non-random distribution. Such findings reiterate the need to combine field and molecular approaches when using fecal samples to survey communities, and underscore the need for broader studies of the carnivore communities of Pakistan.

Keywords

Distribution Carnivores Molecular ecology Fecal DNA 

Notes

Supplementary material

13364_2019_428_MOESM1_ESM.csv (1 kb)
ESM 1 (CSV 726 bytes)

References

  1. Akrim F, Mahmood T, Max T, Nadeem MS, Qasim S, Andleeb S (2018) Assessment of bias in morphological identification of carnivore scats confirmed with molecular scatology in north-eastern Himalayan region of Pakistan. PeerJ 6:52–62CrossRefGoogle Scholar
  2. Anwar MB, Jackson R, Nadeem MS, Janečka JE, Hussain S, Beg MA, Muhammad G, Qayyum M (2011) Food habits of the snow leopard Panthera uncia (Schreber, 1775) in Baltistan, northern Pakistan. Eur J Wildl Res 57:1077–1083CrossRefGoogle Scholar
  3. Archie EA, Moss CJ, Alberts SC (2003) Characterization of tetranucleotide microsatellite loci in the African Savannah Elephant (Loxodonta africana africana). Mol Ecol Notes 3(2):244–246CrossRefGoogle Scholar
  4. Atwood TC, Gese EM (2010) Importance of resource selection and social behavior to partitioning of hostile space by sympatric canids. J Mammal 91:490–499CrossRefGoogle Scholar
  5. Beja-Pereira A, Oliveira R, Alves PC, Schwartz MK, Luikart G (2009) Advancing ecological understandings through technological transformations in noninvasive genetics. Mol Ecol Res 9:1279–1301CrossRefGoogle Scholar
  6. Bell JR (2008) A simple way to treat PCR products prior to sequencing using ExoSAP-IT. Biotech 44:834CrossRefGoogle Scholar
  7. Carroll EL, Bruford MW, DeWoody JA, Leroy G, Strand A, Waits L, Wang J (2018) Genetic and genomic monitoring with minimally invasive sampling methods. Evol Appl 11:1094–1119CrossRefGoogle Scholar
  8. Ceballos G, Erlich PR, Soberon J, Salazar I, Fay JP (2005) Global mammal conservation: what must we manage? Science 309:603–607CrossRefGoogle Scholar
  9. Davison A, Birks JDS, Brookes RC, Braithwaite RC, Messenger JE (2002) On the origin of faeces: morphological versus molecular methods for surveying rare carnivores from their scats. J Zool 257:141–143CrossRefGoogle Scholar
  10. Eggert JA, Woodruff DS (2003) Estimating population sizes for elusive animals: the forest elephants of Kakum National Park, Ghana. Mol Ecol 12:1389–1402CrossRefGoogle Scholar
  11. Farkas A, Jánoska F, Fodor JT, Náhlik A (2017) The high level of nutritional niche overlap between red fox (Vulpes vulpes) and sympatric golden jackal (Canis aureus) affects the body weight of juvenile foxes. Eur J Wildl Res 63:46Google Scholar
  12. Farrell LE, Roman J, Sunquist ME (2000) Dietary separation of sympatric carnivores identified by molecular analysis of scats. Mol Ecol 9:1583–1590CrossRefGoogle Scholar
  13. Gompper ME, Kays RW, Ray JC, LaPoint SD, Bogan DA, Cryan JR (2006) A comparison of non-invasive techniques to survey carnivore communities in northeastern North America. Wildl Soc Bull 34:1142–1151CrossRefGoogle Scholar
  14. GOP (2006) Meterological data of Rawalpindi from 1931 to 2006. Pakistan. http://www.met.gov.pk/cdpc/islamabad.htm. Accessed April 2017
  15. Gutema TM, Atickem A, Bekele A, Sillero-Zubiri C, Kasso M, Tsegaye D, Venkataraman VV, Fashing PJ, Zinner D, Stenseth NC (2018) Competition between sympatric wolf taxa: an example involving African and Ethiopian wolves. R Soc Open Sci 5:172207CrossRefGoogle Scholar
  16. Hinton JW, Proctor C, Kelly MJ, van Manen FT, Vaughan MR, Chamberlain MJ (2016) Space use and habitat selection by resident and transient red wolves (Canis rufus). PLoS One 1112:167–603Google Scholar
  17. Jackson R, Hunter DO (1996) Snow leopard survey and conservation handbook. International Snow Leopard Trust, Seattle, Washington and U.S. Geological Survey, Fort Collins Science Center, Colorado 154 ppGoogle Scholar
  18. Kabir M, Hameed S, Ali H, Bosso L, Din JU, Bischof R, Redpath S, Nawaz MA (2017) Habitat suitability and movement corridors of grey wolf (Canis lupus) in northern Pakistan. PLoS One 12:0187–0027Google Scholar
  19. Kelly MJ, Betsch J, Wultsch C, Mesa B, Mills LS (2012) Non invasive sampling for carnivores. In: Boitani L, Powell R (eds) Carnivore ecology and conservation: a handbook of techniques. Oxford University Press, pp 49–69Google Scholar
  20. Kessing BD, Martin CA, McIntosh C, McMillan MO, Palumbi S (1989) The simple fool’s guide to PCR. University of Hawaii, pp 24Google Scholar
  21. Khan LA (1994) Working plan for coniferous forest of Murree and Kahuta Tehsils of Rawalpindi District. Development and Working Plan Circle 2, LahoreGoogle Scholar
  22. Kindberg J, Ericsson G, Swenson JE (2009) Monitoring rare or elusive large mammals using effort-corrected voluntary observers. Biol Conserv 142:159–165Google Scholar
  23. Kocher TD, Thomas WK, Meyer A, Edwards SV, Paabo S, Villablanca FX, Wilson AC (1989) Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. Proc Natl Acad Sci U S A 86:6196–6200CrossRefGoogle Scholar
  24. Laguardia A, Wang J, Leishi F, Shi K, Priordan P (2009) Species identification refined by molecular scatology in a community of sympatric carnivores in Xinjiang, China. Zool Res 36:72–78Google Scholar
  25. Lesmeister DB, Nielsen CK, Schauber EM, Hellgren EC (2015) Spatial and temporal structure of a mesocarnivore guild in Midwestern North America. Wildl Monog 191:1–61CrossRefGoogle Scholar
  26. Litvaitis JA (2000) Investigating food habits of terrestrial vertebrates. In: Boitani L, Fuller TK (eds) Research techniques in animal ecology. Columbia University Press, New York Press, pp 165–190Google Scholar
  27. Longinger RC, Gese EM, Waits LP (2015) Evaluating the reliability of field identification and morphometric classifications for carnivore scats confirmed with genetic analysis. Wildl Soc Bull 39:593–602CrossRefGoogle Scholar
  28. MacKay P, Zielinski WJ, Long RA, Ray JC (2008) Noninvasive research and carnivore conservation. In: Long RA, Mackay P, Zielinski WJ, Ray JC (eds) Noninvasive survey methods for carnivores. Island Press, Washington D.C, pp 1–7Google Scholar
  29. Mittermeier RA, Myers N, Thomsen JB, Dafonesca GAB, Oliveri S (1998) Biodiversity hotspots and major tropical wilderness areas: approaches to setting conservation priorities. Conserv Biol 12:516–520CrossRefGoogle Scholar
  30. Mohammadi A, Kaboli M, López-Bao JV (2017) Interspecific killing between wolves and golden jackals in Iran. Eur J Wildl Res 63:61CrossRefGoogle Scholar
  31. Monterroso P, Castro D, Silva TL, Ferreras P, Godinho R, Alves PC (2013) Factors affecting the (in) accuracy of mammalian mesocarnivore scat identification in south-western Europe. J Zool 289:243–250CrossRefGoogle Scholar
  32. Morin DJ, Higdon SD, Holub JL, Montague DM, Fies ML, Waits LP, Kelly MJ (2016) Bias in carnivore diet analysis resulting from misclassification of predator scats based on field identification. Wildl Soc Bull 40:669–677CrossRefGoogle Scholar
  33. Palomares F, Godoy JA, Piriz A, Obrien SJ, Johnson WE (2002) Faecal genetic analysis to determine the presence and distribution of elusive carnivores: design and feasibility for the Iberian lynx. Mol Ecol 11:2171–2182CrossRefGoogle Scholar
  34. Panasci M, Ballard WB, Breck S, Rodriguez D, Densmore LD, Wester DB, Baker RJ (2011) Evaluation of fecal DNA preservation techniques and effects of sample age and diet on genotyping success. J Wildl Manag 75:1616–1624CrossRefGoogle Scholar
  35. Perez I, Geffen E, Mokady O (2006) Critically endangered Arabian leopards Panthera pardus nimr in Israel: estimating population parameters using molecular scatology. Oryx 40:295–301CrossRefGoogle Scholar
  36. Putman RJ (1984) Facts from faeces. Mammal Rev 14:79–97CrossRefGoogle Scholar
  37. Roberts TJ (1997) The mammals of Pakistan. Oxford University Press, Karachi 525 ppGoogle Scholar
  38. Russello MA, Waterhouse MD, Etter PD, Johnson EA (2015) From promise to practice: pairing non-invasive sampling with genomics in conservation. PeerJ 3:e1106CrossRefGoogle Scholar
  39. Salek M, Cervinka J, Padyšáková E, Kreisinger J (2014) Does spatial co-occurrence of carnivores in a Central European agricultural landscape follow the null model? Eur J Wildl Res 60(1):99–107Google Scholar
  40. Shehzad W, Riaz T, Nawaz MA, Miquel C, Poillot C, Shah SA, Pompanon F, Coissac E, Taberlet P (2012) Carnivore diet analysis based on next-generation sequencing: application to the leopard cat (Prionailurus bengalensis) in Pakistan. Mol Ecol 21:1951–1965CrossRefGoogle Scholar
  41. Sheikh KM, Molur S (2004) Status and red list of Pakistan’s mammals. Based on the conservation assessment and management plan. IUCN Pakistan, IslamabadGoogle Scholar
  42. Siddiqui MF, Ahmed M, Khan N, Khan IA (2010) A quantitative description of moist temperate conifer forests of Himalaya region of Pakistan and Azad Kashmir. Int J Biol 7(3):175–185Google Scholar
  43. Soto C, Palomares F (2015) Coexistence of sympatric carnivores in relatively homogeneous Mediterranean landscapes: functional importance of habitat segregation at the fine scale level. Oecologia 179(1):223–235CrossRefGoogle Scholar
  44. Tsunoda H, Ito K, Peeva S, Raichev E, Kaneko Y (2018) Spatial and temporal separation between the golden jackal and three sympatric carnivores in a human-modified landscape in central Bulgaria. Zool Ecol 28(3):172–179CrossRefGoogle Scholar
  45. Vanak AT, Gompper ME (2010) Interference competition at the landscape level: the effect of free-ranging dogs on a native mesocarnivore. J Appl Ecol 47:1225–1232CrossRefGoogle Scholar
  46. Waits LP, Paetkau D (2005) Noninvasive genetic sampling tools for wildlife biologists: a review of applications and recommendations for accurate data collection. J Wildl Manag 69:1419–1433CrossRefGoogle Scholar

Copyright information

© Mammal Research Institute, Polish Academy of Sciences, Białowieża, Poland 2019

Authors and Affiliations

  • Rukhsana Khatoon
    • 1
    Email author
  • Tariq Mehmood
    • 1
  • Maqsood Anwar
    • 1
  • Ume Habiba
    • 1
  • Lori S. Eggert
    • 2
  • Matthew E. Gompper
    • 3
  1. 1.Department of Wildlife ManagementPMAS-University of Arid AgricultureRawalpindiPakistan
  2. 2.Division of Biological SciencesUniversity of MissouriColumbiaUSA
  3. 3.School of Natural ResourcesUniversity of MissouriColumbiaUSA

Personalised recommendations