Challenges in the use of genetic mark-recapture to estimate the population size of Bwindi mountain gorillas (Gorilla beringei beringei)

Biological Conservation

Volumn 180, Issue , 2014, Pages 249-261

  Roy, Justin ^a   Vigilant, Linda ^a   Gray, Maryke ^b   Wright, Edward ^a   Kato, Raymond ^c   Kabano, Peter ^a   Basabose, Augustin ^b   Tibenda, Emmanuel ^d,e   Kühl, Hjalmar S ^a   Robbins, Martha M ^a  

^a MAX PLANCK INSTITUTE FOR EVOLUTIONARY ANTHROPOLOGY   (Germany)

^b International Gorilla Conservation Programme   (Rwanda)

^c UGANDA WILDLIFE AUTHORITY   (Uganda)

^d Institute for Tropical Forest Conservation   (Uganda)

^e WILDLIFE CONSERVATION SOCIETY   (United States)

Author keywords

Detection probability; Genetic census; Genotyping; Noninvasive samples

Indexed keywords

CENSUS; CONSERVATION MANAGEMENT; COST ANALYSIS; DETECTION METHOD; ENDANGERED SPECIES; FECAL PELLET; GENETIC ANALYSIS; GENOTYPE; MARK-RECAPTURE METHOD; MONITORING; POPULATION DYNAMICS; POPULATION ESTIMATION; POPULATION SIZE; PRIMATE;

BWINDI IMPENETRABLE NATIONAL PARK; UGANDA;

GORILLA GORILLA BERINGEI;

EID: 84908672742     PISSN: 00063207     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biocon.2014.10.011     Document Type: Article

References (46)

1. Arandjelovic M., Guschanski K., Schubert G., Harris T.R., Thalmann O., Siedel H., Vigilant L. Two-step multiplex polymerase chain reaction improves the speed and accuracy of genotyping using DNA from noninvasive and museum samples. Mol. Ecol. Resour. 2009, 9:28-36. 10.1111/j.1755-0998.2008.02387.x.
2. Arandjelovic M., Head J., Kühl H., Boesch C., Robbins M.M., Maisels F., Vigilant L. Effective non-invasive genetic monitoring of multiple wild western gorilla groups. Biol. Conserv. 2010, 143:1780-1791. 10.1016/j.biocon.2010.04.030.
3. Arandjelovic Mimi, Head Josephine, Rabanal L.I., Schubert Grit, Mettke E., Boesch Christophe, Robbins Martha M., Vigilant Linda Non-invasive genetic monitoring of wild central chimpanzees. PLoS ONE 2011, 6:e14761. 10.1371/journal.pone.0014761.
4. Arrendal J., Vilà C., Björklund M. Reliability of noninvasive genetic census of otters compared to field censuses. Conserv. Genet. 2007, 8:1097-1107. 10.1007/s10592-006-9266-y.
5. Boulanger J., White G.C., McLellan B.N., Woods J., Proctor M., Himmer S. A meta-analysis of grizzly bear DNA mark-recapture projects in British Columbia, Canada. Ursus 2002, 13:137-152.
6. Bradley B.J., Boesch Christophe, Vigilant Linda Identification and redesign of human microsatellite markers for genotyping wild chimpanzee (Pan troglodytes verus) and gorilla (Gorilla gorilla gorilla) DNA from faeces. Conserv. Genet. 2000, 1:289-292.
7. Bradley B.J., Chambers K.E., Vigilant Linda Accurate DNA-based sex identification of apes using non-invasive samples. Conserv. Genet. 2001, 2:179-181.
8. Burnham K., Anderson D. Model selection and multimodel inference - A practical information-theoretic approach 2002, Springer, New York, USA. 2nd ed.
9. Gray Maryke, McNeilage A., Fawcett K., Robbins Martha M., Ssebide B., Mbula D., Uwingeli P. Censusing the mountain gorillas in the Virunga Volcanoes: complete sweep method versus monitoring. Afr. J. Ecol. 2009, 48:588-599. 10.1111/j.1365-2028.2009.01142.x.
10. Gray Maryke, Roy J., Vigilant Linda, Fawcett K., Basabose A., Cranfield M., Uwingeli P., Mburanumwe I., Kagoda E., Robbins Martha M. Genetic census reveals increased but uneven growth of a critically endangered mountain gorilla population. Biol. Conserv. 2013, 158:230-238. 10.1016/j.biocon.2012.09.018.
11. Guerrera W., Sleeman J.M., Jasper S.B., Lonny B., Ichinose T.Y., Reif J.S. Medical survey of the local human population to determine possible health risks to the mountain gorillas of Bwindi Impenetrable Forest National Park, Uganda. Int. J. Primatol. 2003, 24:197-207.
12. Guschanski Katerina, Vigilant Linda, McNeilage A., Gray Maryke, Kagoda E., Robbins Martha M. Counting elusive animals: comparing field and genetic census of the entire mountain gorilla population of Bwindi Impenetrable National Park, Uganda. Biol. Conserv. 2009, 142:290-300. 10.1016/j.biocon.2008.10.024.
13. Harris R.B., Winnie J., Amish S.J., Beja-Pereira A., Godinho R., Costa V., Luikart Gordon Argali abundance in the Afghan Pamir using capture-recapture modeling from fecal DNA. J. Wildlife Manage. 2010, 74:668-677. 10.2193/2009-292.
14. Head J.S., Boesch C., Robbins M.M., Rabanal L.I., Makaga L., Kühl H.S. Effective sociodemographic population assessment of elusive species in ecology and conservation management. Ecol. Evolut. 2013, 3:2903-2916. 10.1002/ece3.670.
15. Kalinowski S.T., Taper M.L., Marshall T.C. Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol. Ecol. 2007, 16:1099-1106. 10.1111/j.1365-294X.2007.03089.x.
16. Katzner T.E., Ivy J.A.R., Bragin E.A., Milner-Gulland E.J., DeWoody J.A. Conservation implications of inaccurate estimation of cryptic population size. Anim. Conserv. 2011, 14:328-332. 10.1111/j.1469-1795.2011.00444.x.
17. Kendall W.L., Pollock K.H., Brownie C., Kendall W.L. A likelihood-based approach to capture-recapture estimation of demographic parameters under the robust design. Biometrics 1995, 51:293-308.
18. Kühl H.S., Burghardt T. Animal biometrics: quantifying and detecting phenotypic appearance. Trends Ecol. Evol. 2013, 28:432-441. 10.1016/j.tree.2013.02.013.
19. Kühl, H.S., Maisels, F., Ancrenaz, M., Williamson, E.A., 2008. Best practice guidelines for surveys and monitoring of great ape populations. IUCN SSC Primate Specialist Group (PSG), Gland, Switzerland.
20. Lampa S., Henle K., Klenke R., Hoehn M., Gruber B. How to overcome genotyping errors in non-invasive genetic mark-recapture population size estimation - a review of available methods illustrated by a case study. J. Wildl. Manag. 2013, 77:1490-1511. 10.1002/jwmg.604.
21. Loos, A., Pfitzer, M., Aporius, L., 2011. Identification of great apes using face recognition. In: 19th European Signal Processing Conference (EUSIPCO). pp. 922-926.
22. Marques F.F.C., Buckland S.T., Goffin D., Dixon C.E., Borchers D.L., Mayle B.A., Peace A.J. Estimating deer abundance from line transect surveys of dung: sika deer in southern Scotland. J. Appl. Ecol. 2001, 38:349-363. 10.1046/j.1365-2664.2001.00584.x.
23. Marucco F., Vucetich L.M., Peterson R.O., Adams J.R., Vucetich J.A. Evaluating the efficacy of non-invasive genetic methods and estimating wolf survival during a ten-year period. Conserv. Genet. 2012, 13:1611-1622. 10.1007/s10592-012-0412-4.
24. McNeilage, A., Plumptre, A.J., Brock-Doyle, A., Vedder, A., 2001. Gorilla Census 1997, Bwindi Impenetrable National Park, Uganda. Oryx 35, pp. 39-47. doi:10.1046/j.1365-3008.2001.00154.x.
25. McNeilage A., Robbins Martha M., Gray Maryke, Olupot W., Babaasa D., Bitariho R., Kasangaki A., Rainer H., Asuma S., Mugiri G., Baker J. Census of the mountain gorilla Gorilla beringei beringei population in Bwindi Impenetrable National Park, Uganda. Oryx 2006, 40:419-427. 10.1017/S0030605306001311.
26. Moore D., Vigilant L. A population estimate of chimpanzees (Pan troglodytes schweinfurthii) in the Ugalla region using standard and spatially explicit genetic capture-recapture methods. Am. J. Primatol. 2014, 76:335-346. 10.1002/ajp.22237.
27. Morgan D., Sanz C., Onononga J.R., Strindberg S. Ape abundance and habitat use in the Goualougo Triangle, Republic of Congo. Int. J. Primatol. 2006, 27:147-179. 10.1007/s10764-005-9013-0.
28. Morin P.A., Mahboubi P., Wedel S., Rogers J. Rapid screening and comparison of human microsatellite markers in baboons: allele size is conserved, but allele number is not. Genomics 1998, 53:12-20. 10.1006/geno.1998.5460.
29. Mowry R.A., Gompper M.E., Beringer J., Eggert L.S. River otter population size estimation using noninvasive latrine surveys. J. Wildl. Manag. 2011, 75:1625-1636. 10.1002/jwmg.193.
30. Murai M., Ruffler H., Berlemont A., Campbell G., Esono F., Agbor A., Mbomio D., Ebana A., Nze A., Kühl H.S. Priority areas for large mammal conservation in Equatorial Guinea. PLoS ONE 2013, 8:e75024. 10.1371/journal.pone.0075024.
31. Nakashima Y., Iwata Y., Ando C., Nze Nkoguee C., Inoue E., Akomo E.-F.O., Nguema P.M., Bineni T.D., Banak L.N., Takenoshita Y., Ngomanda A., Yamagiwa J. Assessment of landscape-scale distribution of sympatric great apes in African rainforests: concurrent use of nest and camera-trap surveys. Am. J. Primatol. 2013, 75:1220-1230. 10.1002/ajp.22185.
32. Nei M. Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 1978, 89:583-590.
33. Nichols J.D., Williams B.K. Monitoring for conservation. Trends Ecol. Evol. 2006, 21:668-673.
34. Nsubuga A.M., Robbins M.M., Roeder A.D., Morin P.A., Boesch C., Vigilant L. Factors affecting the amount of genomic DNA extracted from ape faeces and the identification of an improved sample storage method. Mol. Ecol. 2004, 13:2089-2094. 10.1111/j.1365-294X.2004.02207.x.
35. Otis D.L., Burnham K.P., White G.C., Anderson D.R. Statistical inference from capture data on closed animal populations. Wildlife Monographs 1978, 3-135.
36. Pledger S. Unified maximum likelihood estimates for closed capture-recapture models using mixtures. Biometrics 2000, 56:434-442.
37. Robbins Martha M., Gray Maryke, Kagoda E., Robbins A.M. Population dynamics of the Bwindi mountain gorillas. Biol. Conserv. 2009, 142:2886-2895. 10.1016/j.biocon.2009.07.010.
38. Robbins Martha M., Gray Markye, Fawcett K.A., Nutter F.B., Uwingeli P., Mburanumwe I., Kagoda E., Basabose A., Stoinski T.S., Cranfield M.R., Byamukama J., Spelman L.H., Robbins A.M. Extreme conservation leads to recovery of the Virunga mountain gorillas. PLoS ONE 2011, 6:e19788. 10.1371/journal.pone.0019788.
39. Rowcliffe J.M., Field J., Turvey S.T., Carbone C. Estimating animal density using camera traps without the need for individual recognition. J. Appl. Ecol. 2008, 45:1228-1236. 10.1111/j.1365-2664.2008.0.
40. Spelman L.H., Gilardi K.V.K., Lukasik-Braum M., Kinani J.-F., Nyirakaragire E., Lowenstine L.J., Cranfield M.H. Respiratory disease in mountain gorillas (Gorilla beringei beringe) in Rwanda, 1990-2010: outbreaks, clinical course, and medical management. J. Zoo Wildlife Med. 2013, 44:1027-1035.
41. Waits L. Using noninvasive genetic sampling to detect and estimate abundance of rare wildlife species. Sampling Rare or Elusive Species 2004, 211-228. Island Press, Washington DC, USA. W. Thompson (Ed.).
42. Waits L.P., Luikart G., Taberlet P. Estimating the probability of identity among genotypes in natural populations: cautions and guidelines. Mol. Ecol. 2001, 10:249-256.
43. White G.C., Burnham K.P. Program MARK: survival estimation from populations of marked animals. Bird Study 1999, 46:S120-S139. 10.1080/00063659909477239.
44. Woodford M.H., Butyinski T.M., Karesh W.B. Habituating the great apes: the disease risks. Oryx 2002, 36:153-160. 10.1017/S0030605302000224.
45. Wrege P.H., Rowland E.D., Thompson B.G., Batruch N. Use of acoustic tools to reveal otherwise cryptic responses of forest elephants to oil exploration. Conserv. Biol. 2010, 24:1578-1585. 10.1111/j.1523-1739.2010.01559.x.
46. Zhan X., Li M., Zhang Z., Goossens B., Chen Y., Wang H., Bruford M.W., Wei F. Molecular censusing doubles giant panda population estimate in a key nature reserve. Curr. Biol. 2006, 16:R451-2. 10.1016/j.cub.2006.05.042.