Influence of habitat fragmentation on the genetic structure of large mammals: Evidence for increased structuring of African buffalo (Syncerus caffer) within the Serengeti ecosystem

Conservation Genetics

Volumn 13, Issue 2, 2012, Pages 381-391

  Ernest, E M ^a,b   Haanes, H ^c   Bitanyi, S ^b,d   Fyumagwa, R D ^a   Msoffe, P L ^e   Bjornstad G ^f   Roed K H ^b  

^a TANZANIA WILDLIFE RESEARCH INSTITUTE   (Tanzania)

^b NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

^c NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

^d Ministry of Livestock and Fisheries Development   (Tanzania)

^e SOKOINE UNIVERSITY OF AGRICULTURE   (Tanzania)

^f UNIVERSITY OF OSLO   (Norway)

Author keywords

Conservation; Genetic structure; Microsatellite; Mitochondrial DNA; Tanzania

Indexed keywords

BAYESIAN ANALYSIS; BIOMASS; CATTLE; CONSERVATION GENETICS; ECOTOURISM; GENETIC STRUCTURE; HABITAT CONSERVATION; HABITAT FRAGMENTATION; HERBIVORE; MANAGEMENT PRACTICE; MITOCHONDRIAL DNA; PROTECTED AREA;

ARUSHA [TANZANIA]; MASWA; NGORONGORO CONSERVATION AREA; SERENGETI NATIONAL PARK; SHINYANGA; TANZANIA;

BUBALUS; MAMMALIA; SYNCERUS CAFFER;

EID: 84858007474     PISSN: 15660621     EISSN: 15729737     Source Type: Journal    
DOI: 10.1007/s10592-011-0291-0     Document Type: Article

References (92)

1. Allendorf FW (1986) Genetic drift and the loss of alleles versus heterozygosity. Zoo Biol 5: 181-190.
2. Amos W, Balmford A (2001) When does conservation genetics matter? Heredity 87: 257-265.
3. Bishop MD, Kappes SM, Keele JW, Stone RT, Sunden SLF, Hawkins GA, Toldo SS, Fries R, Grosz MD, Yoo L, Beattie CW (1994) A genetic linkage map for cattle. Genetics 136: 619-639.
4. Boone RB, Galvin KA, Thornton PK, Swift DM, Coughenour MB (2006) Cultivation and conservation in Ngorongoro conservation area, Tanzania. Hum Ecol 34: 809-828.
5. Buchanan FC, Galloway SM, Crawford AM (1993) Ovine microsatellites at the OarFCB11, OarFCB128, OarFCB193, OarFCB266 and OarFCB304 loci. Anim Genet 25: 60.
6. Chakraborty R, Jin L (1993) A unified approach to study hypervariable polymorphisms; statistical considerations of determining relatedness and population distance. EXS 67: 153-175.
7. Chantal S, Tim C, Simon M, Charles M, George S, Markus B (2007) Assessment of effectiveness of protection strategies in Tanzania based on a decade of survey data for large herbivores. Conserv Biol 21: 635-646.
8. Coltman DW (2008) Molecular ecological approaches to studying the evolutionary impact of selective harvesting in wildlife. Mol Ecol 17: 221-235.
9. Conover MR (1997) Monetary and intangible valuation of deer in the United States. Wildl Soc Bull 25: 298-305.
10. Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144: 2001-2014.
11. Cornuet JM, Santos F, Beaumont MA et al (2008) Inferring population history with DIY ABC: a user-friendly approach to approximate Bayesian computation. Bioinformatics 24: 2713-2719.
12. Crawford NG (2010) SMOGD: software for the measurement of genetic diversity. Mol Ecol Resour 10: 556-557.
13. Crawford AM, Dodds KG, Ede AJ, Pierson CA, Montgomery GW, Garmonsway HG, Beattie AE, Davies K, Maddox JF, Kappes SM, Stone RT, Nguyen TC, Penty JM, Lord EA, Broom JE, Buitkamp J, Schwaiger W, Epplen JT, Matthew P, Matthews ME, Hulme DJ, Beh KJ, McGraw RA, Beattie CW (1995) An autosomal genetic linkage map of the sheep genome. Genetics 140: 703-724.
14. Cross PCL, Lloyd JI, Getz WM (2005) Disentangling association patterns in fission-fusion societies using African buffalo as an example. Anim Behav 69: 499-506.
15. DeYoung RW, Honeycutt RL (2005) The molecular toolbox: genetic techniques in wildlife ecology and management. J Wildl Manag 69: 1362-1384.
16. Di Rienzo A, Peterson AC, Garza JC (1994) Mutational processes of simple-sequence repeat loci in human population. Proc Natl Acad Sci USA 91: 3166-3170.
17. El Mousadik A, Petit RJ (1996) High level of genetic differentiation for allelic richness among populations of the argan tree [Argania spinosa (L. Skeels)] endemic to Morocco. Theor Appl Genet 92: 832-839.
18. Estes RD (1991) The behaviour guide to African mammals. The University of California Press, Berkeley.
19. Estes RD, Atwood JL, Estes AB (2006) Downward trends in Ngorongoro Crater ungulate populations 1986-2005: conservation concerns and the need for ecological research. Biol Conserv 131: 106-120.
20. Estoup A, Jarne PJ, Cornuet JM (2002) Homoplasy and mutation model at microsatellite loci and their consequences for population genetic analysis. Mol Ecol 11: 1591-1604.
21. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14: 2611-2620.
22. Excoffier L, Laval G, Schneider S (2005) Arlequin 3. 01: an integrated software package for population genetics data analysis. Evol Bioinformatics Online 1: 47-50.
23. Filatov DA (2002) Proseq: a Software for preparation and evolutionary analysis of DNA sequence data sets. Mol Ecol Notes 2: 621-624.
24. Flagstad Ø, Syvertsen PO, Stenseth NC, Stacy JD, Olsaker I, Røed KH, Jakobsen KS (2000) Genetic variability in Swayne's Hartebeest, an endangered antelope of Ethiopia. Conserv Biol 14: 254-264.
25. Frankham R (1995) Effective population size/adult population size ratios in wildlife: a review. Genet Res Camb 66: 95-107.
26. Frankham R (1996) Relationship of genetic variation to population size in wildlife. Conserv Biol 10: 1500-1508.
27. Fu YX, Chakraborty R (1998) Simultaneous estimation of all the parameters of a stepwise mutation model. Genetics 150: 487-497.
28. Fynn RWS, Bonyongo MC (2010) Functional conservation areas and the future of Africa's wildlife. Afr J Ecol 49: 175-188.
29. Fyumagwa RD, Runyoro V, Horak IG, Hoare R (2007) Ecology and control of ticks as disease vectors in wildlife in Ngorongoro Crater, Tanzania. S Afr J Wildl Res 37: 79-90.
30. Gaggiotti OE, Lange O, Rassmann K, Gliddon C (1999) A comparison of two indirect methods for estimating average levels of gene flow using microsatellite data. Mol Ecol 8: 1513-1520.
31. Galvin KA, Thornton PK, Boone RB, Sunderland (2004) Climate variability and impacts on east African livestock herders: the Maasai of Ngorongoro conservation area, Tanzania. Afr J Range Forage Sci 21: 183-189.
32. Garza JC, Williamson EG (2001) Detection of reduction in population size using data from microsatellite loci. Mol Ecol 10: 305-318.
33. George AR (1975) Buffalo increase and seasonal use of Ngorongoro Crater. E Afr Wildl J 13: 385-387.
34. Goldstein DB, Ruiz-Linares A, Cavalli-Sforza LL, Feldman MW (1995) An evaluation of genetic distances for use with microsatellite loci. Genetics 139: 463-471.
35. Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices. Release 2. 9. 3. 2. Available via http://www. unil. ch/izea/softwares/fstat. html. Accessed on 2009.
36. Grant PR, Grant BR (1992) Demography and the genetically effective sizes of two populations of Darwin finches. Ecology 73: 766-784.
37. Halley DJ, Vandewalle MEJ, Mari M, Taolo C (2002) Herd switching and long-distance dispersal in female African buffalo (Syncerus caffer). Afr J Ecol 40: 97-99.
38. Harley EH, Baumgarten I, Cunningham J, O'Ryan C (2005) Genetic variation and population structure in remnant populations of black rhinoceros, Diceros bicornis in Africa. Mol Ecol 14: 2981-2990.
39. Heller R, Lorenzen ED, Okello JBA, Masembe C, Siegismund HR (2008) Mid-Holocene decline in African buffalos inferred from Bayesian coalescent-based analyses of microsatellites and mitochondrial DNA. Mol Ecol 17: 4845-4858.
40. Heller R, Okello JBA, Siegismund H (2010) Can small wildlife conservancies maintain genetically stable populations of large mammals? Evidence for increased genetic drift in geographically restricted populations of Cape buffalo in East Africa. Mol Ecol 19: 1324-1330.
41. Hilborn R, Arcese P, Borner M, Hando J, Hopcraft G, Loibooki M, Mduma S, Sinclair ARE (2006) Effective enforcement in a conservation area. Science 314: 1266.
42. Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Resour 9: 1322-1332.
43. Iain JG, Alison JH, Marco F (2004) The management of wild large herbivores to meet economic, conservation and environmental objectives. J Appl Ecol 41: 1021-1031.
44. Jost L (2008) GST and its relatives do not measure differentiation. Mol Ecol 17: 4015-4026.
45. Kappes SM, Keele JW, Stone RT, McGraw RA, Sonstegard TS, Smith TPL, Lopez-Corrales NL, Beattie CW (1997) A second generation linkage map of the bovine genome. Genome Res 7: 235-249.
46. Keller LF, Waller DM (2002) Inbreeding effects in wild populations. Trends Ecol Evol 17: 230-241.
47. Kemp SJ, Brezinsky L, Teale AJ (1993) A panel of bovine, ovine and caprine polymorphic microsatellites. Anim Genet 25: 363-365.
48. Kijazi A, Mkumbo S, Thompson DM (1997) Human and livestock population trends. In: Thompson DM (ed) Multiple land-use: the experience of the Ngorongoro conservation area, Tanzania. IUCN, Gland, pp 167-180.
49. Kimura M, Crow JF (1964) The number of allele that can be maintained in a finite population. Genetics 49: 725-738.
50. Kimura M, Ohta T (1978) Stepwise mutation model and distribution of allelic frequencies in a finite population. Proc Natl Acad Sci USA 75: 2868-3170.
51. Korte L (2009) Herd-switching in adult female African forest buffalo (Syncerus caffer nanus). Afr J Ecol 47: 125-127.
52. Kurji F (1981) Human population trends within and around the Ngorongoro conservation area: the demographic settings, BRARUP Research Report, No. 44.
53. Kurji F (1985) Population and conservation in the Serengeti-Part 1, Institute of Resource Assessment Research Paper, No. 9.
54. Loibooki M, Hofer H, Campbell K, East LE (2002) Bush meat hunting by communities adjacent to the Serengeti National Park, Tanzania: the importance of livestock ownership and alternative sources of protein and income. Environ Conserv 29: 391-398.
55. Lorenzen ED, Simonsen BOT, Kat PW, Arctander P, Siegismund HR (2006a) Hybridization between subspecies of waterbuck (Kobus ellipsiprymnus) in zones of overlap with limited introgression. Mol Ecol 15: 3787-3799.
56. Lorenzen ED, Arctander P, Siegismund HR (2006b) Regional genetic structuring and evolutionary history of the impala Aepyceros melampus. J Hered 97: 119-132.
57. Lynn S (2000) The effects of conservation policy and ecology on pastoral land use patterns: a case study of Maasai land use in Northern Tanzania. MSc Thesis, Colorado State University, Fort Collins.
58. Marshall TC, Slate J, Kruuk LEB, Pemberton JM (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7: 639-655.
59. McCabe JT, Mollel N, Tumaini A (1997) Food security and the role of cultivation. In: Thompson DM (ed) Multiple land-use: the experience of the Ngorongoro conservation area, Tanzania. IUCN, Gland, pp 397-416.
60. McNaughton SJ, Campbell K (1991) Long-term ecological research in African ecosystems. In: Risser PG (ed) Long-term research. Wiley, Chichester, pp 173-189.
61. Meertens HCC, Ndege LJ, Enserink HJ (1995) Dynamics in farming systems: changes in time and space in Sukumaland. Royal Tropical Institute, Arusha.
62. Metzger KL, Sinclair ARE, Hilborn R, Hopcraft JGC (2010) Evaluating the protection of wildlife in parks: the case of African buffalo in Serengeti. Biodivers Conserv 19: 3431-3444.
63. NCAA (Ngorongoro Conservation Area Authority) (1999) 1998 Aerial boma count, 1999 people and livestock census, and human population trend between 1954 and 1999 in the NCA. Research and Planning Unit. Ngorongoro Conservation Area Authority, Ngorongoro Crater.
64. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York.
65. Neumann RP (1998) Imposing wilderness: struggles over livelihood and nature preservation in Africa. University of California, Berkeley.
66. Newmark WD (2008) Isolation of African protected areas. Front Ecol Environ 6: 321-328.
67. O'Ryan C, Harley EH, Bruford MW, Beaumont M, Wayne RK, Cherry MI (1998) Microsatellite analysis of genetic diversity in fragmented South African buffalo populations. Anim Conserv 1: 85-94.
68. Ogutu ZA (2002) The impact of ecotourism on livelihood and natural resource management in Eselenkei, Amboseli ecosystem, Kenya. Land Degrad Dev 13: 251-256.
69. Okello JBA, Wittemyer G, Rasmussen HB, Arctander P, Nyakaana S, Douglas-Hamilton I, Siegismund HR (2008) Effective population size dynamics reveal impacts of historic climatic events and recent anthropogenic pressure in African elephants. Mol Ecol 17: 3788-3799.
70. Prins HHT (1996) Ecology and behaviour of the African buffalo. Social inequality and decision making. Champman and Hall, London.
71. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155: 945-959.
72. Ralph K, Karin EH, Otto H, Josef S, Bernhard S, Christoph S (2006) Genetic effect of transportation infrastructure on Roe Deer populations (Capreolus capreolus). J Hered 98: 13-22.
73. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43: 223-225.
74. Rousset F (2008) GenePop'007: a complete re-implementation of the GenePop software for Windows and Linux. Mol Ecol Resour 8: 103-106.
75. Runyoro V, Hofer H, Chausi EB, Moehlman PD (1995) Long-term trends in the herbivore population of the Ngorongoro Crater, Tanzania. In: Sinclair ARE, Arcese P (eds) Serengeti II dynamics management and conservation of an ecosystem. University of Chicago Press, Chicago, pp 146-168.
76. Sidney J (1965) The past and present distribution of some African ungulates. Trans Zool Soc Lond 30: 1-397.
77. Simonsen BT, Siegismund HR, Arctander P (1998) Population structure of African buffalo inferred from mtDNA sequences and microsatellite loci: high variation but low differentiation. Mol Ecol 7: 225-237.
78. Sinclair ARE (1977) In: George BS (ed) The African buffalo, a study of resource limitation of population. Chicago University Press, Chicago, p 355.
79. Solinas TS, Fries R (1993) Physically mapped, cosmid-derived microsatellite markers as anchor loci on bovine chromosomes. Mamm Genome 4: 720-727.
80. Songorwa AN (2004) Human population increase and wildlife conservation in Tanzania: Are the wildlife managers addressing the problem or treating symptoms? AJEAM-RAGEE 9: 49-77.
81. Soulé ME, Mills S (1992) Conservation genetics and conservation biology: a troubled marriage. In: Sandlund OT, Hindar K, Brown AHD (eds) Conservation of biodiversity for sustainable development. Scandinavian University Press, Oslo, pp 55-69.
82. Stuwart SN, Adams RJ, Jenkins MD (1990) Biodiversity in sub-Sahara Africa and its islands. IUCN-SSC No. 6 IUCN. University of Chicago Press, Glands.
83. TAWIRI (2008) Aerial census in the Serengeti ecosystem, wet season report, TAWIRI aerial survey report.
84. Thirgood S, Anna M, Sebastian T, Grant H, Ephraim M, Titus M, Morris K, John F, Sinclair ARE, Markus B (2004) Can parks protect migratory ungulates? The case of the Serengeti wildebeest. Anim Conserv 7: 113-120.
85. van Hooft WF, Groen AF, Prins HHT (2000) Microsatellite analysis of genetic diversity in African buffalo (Syncerus caffer) populations throughout Africa. Mol Ecol 9: 2017-2025.
86. van Hooft WF, Groen AF, Prins HHT (2002) Phylogeography of the African buffalo based on mitochondrial and y-chromosomal loci: pleistocene origin and population expansion of the Cape buffalo subspecies. Mol Ecol 11: 267-279.
87. van Hooft WF, Groen AF, Prins HHT (2003) Genetic structure of African buffalo herds based on variation at the mitochondrial D-loop and autonomic microsatellite loci: evidence for male-biased gene flow. Conserv Genet 4: 467-477.
88. van Oosterhout C, Hutchinson WF, Wills DP, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4: 535-538.
89. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38: 1358-1370.
90. Wenink PW, Groen AF, Roelke-Parker ME, Prins HHT (1998) African buffalo maintaining high genetic diversity in the major histocompatibility complex in spite of historically known population bottlenecks. Mol Ecol 7: 1315-1322.
91. World Resources Institute (Cited as WRI) (1989) An assessment of the resource base that supports the global economy. Basic Books Inc., New York.
92. Wright S (1931) Evolution in Mendelian populations. Genetics 16: 97-159.