Wetlands are keystone habitats for jaguars in an intercontinental biodiversity hotspot


Autoři: Joe J. Figel aff001;  Sebastián Botero-Cañola aff002;  German Forero-Medina aff004;  Juan David Sánchez-Londoño aff005;  Leonor Valenzuela aff004;  Reed F. Noss aff007
Působiště autorů: Department of Biology, University of Central Florida, Orlando, Florida, United States of America aff001;  Harold W Manter Laboratory of Parasitology, University of Nebraska State Museum and School of Biological Sciences, University of Nebraska, Lincoln, Nebraska, United States of America aff002;  Instituto de Biología, Grupo de Mastozoología, Universidad de Antioquia, Medellín, Colombia aff003;  Wildlife Conservation Society-Colombia Program, Cali, Colombia aff004;  Facultad de Ciencias y Biotecnología, Universidad CES, Medellín, Colombia aff005;  Fundación BioDiversa, Bogotá, Colombia aff006;  Florida Institute for Conservation Science, Chuluota, Florida, United States of America aff007
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0221705

Souhrn

Agricultural development was the major contributor to South America’s designation as the continent with the highest rates of forest loss from 2000–2012. As the apex predator in the Neotropics, jaguars (Panthera onca) are dependent on forest cover but the species’ response to habitat fragmentation in heterogeneous agricultural landscapes has not been a subject of extensive research. We used occupancy as a measure of jaguar habitat use in Colombia’s middle Magdalena River valley which, as part of the intercontinental Tumbes-Chocó-Magdalena biodiversity hotspot, is exceedingly fragmented by expanding cattle pastures and oil palm plantations. We used single-season occupancy models to analyze 9 months of data (2015–2016) from 70 camera trap sites. Given the middle Magdalena’s status as a “jaguar corridor” and our possible violation of the occupancy models’ demographic closure assumption, we interpreted our results as “probability of habitat use (Ψ)” by jaguars. We measured the associations between jaguar presence and coverage of forest, oil palm, and wetlands in radii buffers of 1, 3, and 5 km around each camera trap. Our camera traps recorded 77 jaguar detections at 25 of the camera trap sites (36%) during 15,305 trap nights. The probability of detecting jaguars, given their presence at a site, was 0.28 (0.03 SE). In the top-ranked model, jaguar habitat use was positively influenced by wetland coverage (β = 7.16, 3.20 SE) and negatively influenced by cattle pastures (β = -1.40, 0.63 SE), both in the 3 km buffers. We conclude that wetlands may serve as keystone habitats for jaguars in landscapes fragmented by cattle ranches and oil palm plantations. Greater focus on wetland preservation could facilitate jaguar persistence in one of the most important yet vulnerable areas of their distribution.

Klíčová slova:

Biology and life sciences – Organisms – Eukaryota – Animals – Vertebrates – Amniotes – Mammals – Cats – Jaguars – Plants – Oil palm – Ecology – Ecosystems – Forests – Ecology and environmental sciences – Aquatic environments – Freshwater environments – Wetlands – Terrestrial environments – Habitats – Earth sciences – Marine and aquatic sciences – Geomorphology – Topography – Landforms – Valleys – Hydrology – Flooding – People and places – Geographical locations – South America – Colombia


Zdroje

1. Hansen MC, Potapov PV, Moore R, Hancher M, Turubanova SA, Tyukavina A, et al. High resolution global maps of 21st century forest cover change. Science. 2013; 342: 850–853. doi: 10.1126/science.1244693 24233722

2. Ripple WJ, Estes JA, Beschta RL, Wilmers CC, Ritchie EG, Hebblewhite M, et al. Status and ecological effects of the world’s largest carnivores. Science. 2014; 343: 151–163.

3. Treves A, Karanth KU. Human-carnivore conflict and perspectives on carnivore management worldwide. Conserv Biol. 2003; 17: 1491–1499.

4. Goldstein I, Paisley S, Wallace RB, Jorgenson JP, Cuesta F, Castellanos A. Andean bear-livestock conflicts: A review. Ursus. 2006; 17: 8–15.

5. Kattan G, Lucía-Hernández O, Goldstein I, Rojas V, Murillo O, Gómez C, et al. Range fragmentation of the spectacled bear in the northern Andes. Oryx. 2004; 38: 155–163.

6. Rabinowitz A, Zeller K. A range-wide model of landscape connectivity and conservation for the jaguar. Biol Conserv. 2010; 143: 939–945.

7. de la Torre JA, Núñez JM, Medellín RA. Habitat availability and connectivity for jaguars in the Southern Mayan Forest: Conservation priorities for a fragmented landscape. Biol Conserv. 2017; 206: 270–282.

8. Tobler MW, Powell, GVN. Estimating jaguar densities with camera traps: Problems with current designs and recommendations for future studies. Biol Conserv. 2013; 159: 109–118.

9. Quigley HB, Crawshaw Jr. PG. A conservation plan for the jaguar in the Pantanal region of Brazil. Biol Conserv. 1992; 61: 149–157.

10. Silveira L, Sollmann R., Jácomo ATA, Diniz-Filho JAF, Torres NM. The potential for large-scale wildlife corridors between protected areas in Brazil using the jaguar as a model species. Landsc Ecol. 2014; 29: 1213–1223.

11. Sanderson EW, Redford KH, Chetkiewicz CB, Medellin RA, Rabinowitz A, Robinson JG, et al. Planning to save a species: the jaguar as a model. Conserv Biol. 2002; 16: 1–15.

12. Zeller K. Jaguars in the new millennium data set update: the state of the jaguar in 2006. New York: Wildlife Conservation Society; 2007.

13. Morato RG, Stabach JA, Fleming CH, Calabrese JM, de Paula RC, Ferraz KMPM, et al. Space use and movement of a Neotropical top predator: the endangered jaguar. PLoS ONE. 2016; 11: e0168176. doi: 10.1371/journal.pone.0168176 28030568

14. Karanth KU, Nichols JD, Kumar NS, Link WA, Hines JE. Tigers and their prey: predicting carnivore densities from prey abundance. Proc Natl Acad Sci U.S.A. 2004; 101: 4854–4858. doi: 10.1073/pnas.0306210101 15041746

15. Duangchatrasiri S, Jornburom P, Jinamoy S, Pattanvibool A, Hines JE, Arnold TW, et al. Impact of prey occupancy and other ecological and anthropogenic factors on tiger distribution in Thailand’s western forest complex. Ecol Evol. 2019; 9: 2449–2458. doi: 10.1002/ece3.4845 30891192

16. Santos F, Carbone C, Wearn OR, Rowcliffe JM, Espinosa S, Lima MGM, et al. Prey availability and temporal partitioning modulate felid coexistence in Neotropical forests. PLoS ONE. 2019; 14: e0213671. doi: 10.1371/journal.pone.0213671 30861045

17. Rabelo RM, Aragon S, Bicca-Marques JC. Prey abundance drives habitat occupancy by jaguars in Amazonian floodplain river islands. Acta Oecol. 2019; 97: 28–33.

18. Hayward MW, Kamler JF, Montgomery RA, Newlove A, Rostro-Garcia S, Sales LP, et al. Prey preferences of the jaguar reflect the post-Pleistocene demise of large prey. Front Ecol Evol. 2016; 3: 148.

19. Emmons LH. Comparative feeding ecology of felids in a Neotropical forest. Behav Ecol Sociobiol. 1987; 20: 271–283.

20. Scognamillo D, Maxit IE, Sunquist M, Polisar J. Coexistence of jaguar and puma in a mosaic landscape in the Venezuelan llanos. J Zool. 2003; 259: 269–279.

21. Foster RJ, Harmsen BJ, Valdes B, Pomilla C, Doncaster CP. Food habits of sympatric jaguars and pumas across a gradient of human disturbance. Biotropica. 2010; 280: 309–318.

22. Cavalcanti SMC, Gese EM. Kill rates and predation patterns of jaguars in the southern Pantanal, Brazil. J Mamm. 2010; 91: 722–736.

23. Emmons LH. Jaguar predation on chelonians. J Herpetol. 1989; 23: 311–314.

24. Zuloaga JG. Densidad de población, hábitos alimenticios y anotaciones sobre habitat natural del jaguar en la depression inundable del bajo San Jorge, Colombia. Título de Biólogo, Universidad Nacional de Colombia, Bogotá. 1995.

25. Da Silveira F, Ramalho EE, Thorbjarnarson J, Magnusson W. Depredation by jaguars on caimans and importance of reptiles in the diet of jaguar. J Herpetol. 2010; 44: 418–424.

26. Azevedo FCC, Verdade LM. Predator-prey interactions: jaguar predation on caiman in a floodplain forest. J Zool. 2012; 286: 200–207.

27. Rodríguez-Mahecha JV, Jorgenson JP, Duran-Ramirez C, Bedoya-Gaitán M. Jaguar Panthera onca. In: Rodriguez JV, Alberico M, Trujillo F, Jorgenson J, editors. Libro Rojo de los Mamíferos de Colombia. Bogotá: Conservación Internacional; 2006. pp. 260–265.

28. Mittermeier RA, Turner WR, Larsen FW, Brooks TM, Gascon C. Global biodiversity conservation: the critical role of hotspots. In: Zachos FE, Habel JC, editors. Biodiversity hotspots: distribution and protection of conservation priority areas. Heidelberg: Springer; 2011. p. 3–22.

29. Etter A, McAlpine C, Wilson K, Phinn S, Possingham H. Regional patterns of agricultural land use and deforestation in Colombia. Agric Ecosyst Environ. 2006; 114: 369–386.

30. Forero-Medina G, Joppa L. Representation of global and national conservation priorities by Colombia’s protected area network. PLoS ONE. 2010: e13210. doi: 10.1371/journal.pone.0013210 20967270

31. Melquist WE. Status survey of otters and spotted cats in Latin America. IUCN Report: 45–253. Idaho Cooperative Wildlife Research Unit. Moscow: University of Idaho; 1984.

32. FEDEPALMA. Anuario Estadístico 2014. La agroindustria de la palma de aceite en Colombia y en el mundo: 2009–2013. Bogotá: FEDEPALMA; 2014.

33. Yue S, Brodie JF, Zipkin EF, Bernard H. Oil palm plantations fail to support mammal diversity. Ecol Appl. 2015; 25: 2285–2292. 26910955

34. Mendes-Oliveira AC, Peres CA, Maués P, Oliveira GL, Mineiro IGB, de Maria SLS, et al. Oil palm monoculture induces drastic erosion of an Amazonian forest mammal fauna. PLoS ONE. 2017; 12: e0187650. doi: 10.1371/journal.pone.0187650 29117202

35. Meijaard E, Garcia-Ulloa J, Sheil D, Wich SA, Carlson KM, Juffe-Bignoli D, et al. Oil palm and biodiversity. A situation analysis by the IUCN Oil Palm Task Force. Gland Switzerland: IUCN; 2018.

36. FAO. FAOSTAT Online Statistical Service. Food and Agricultural Organization of the United Nations. 2016. Available from http://faostat3.fao.org (accessed December 2018)

37. Borron V, Tzanopoulos J, Gallo J, Barragan J, Jaimes-Rodriguez L, Schaller GB, et al. Jaguar densities across human-dominated landscapes in Colombia: the contribution of unprotected areas to long term conservation. PLoS ONE. 2016; 11: e0153973. doi: 10.1371/journal.pone.0153973 27144280

38. Pardo LE, Campbell MJ, Edwards W, Clements GR, Laurance WF. Terrestrial mammal responses to oil palm dominated landscapes in Colombia. PLoS ONE. 2018; 13: e0197539. doi: 10.1371/journal.pone.0197539 29795615

39. Olsoy PJ, Zeller KA, Hicke JA, Quigley HB, Rabinowitz AR, Thornton DH. Quantifying the effects of deforestation and fragmentation on a range-wide conservation plan for jaguars. Biol Conserv. 2016; 203: 8–16.

40. Foster RJ, Harmsen BJ, Doncaster CP. Habitat use by sympatric jaguars and pumas across a gradient of human disturbance in Belize. Biotropica. 2010; 42: 724–731.

41. IDEAM. Zonificación Hidrográfica de Colombia, Escala 1:2.250.000. Bogota. 2013.

42. Mackenzie DI, Royle JA. Designing occupancy studies: General advice and allocating survey effort. J Appl Ecol. 2005; 42: 1105–1114.

43. Moilanan A. Implications of empirical data quality for metapopulation model parameter estimation and application. Oikos. 2002; 96: 516–530.

44. Linkie M, Chapron G, Martyr DJ, Holden J, Leader-Williams N. Assessing the viability of tiger subpopulations in a fragmented landscape. J Appl Ecol. 2006; 43: 576–586.

45. Morato RG, Thompson JJ, Paviolo A, de la Torre JA, Lima F, McBride RT, et al. Jaguar movement database: a GPS-based movement dataset of an apex predator in the Neotropics. Ecology. 2018; 99: 1691. doi: 10.1002/ecy.2379 29961270

46. Ciarniello LM, Boyce MS, Seip DR, Heard DC. Grizzly bear habitat selection is scale dependent. Ecol Appl. 2007; 17: 1424–1440. 17708219

47. Pusparini W, Sievert PR, Fuller TK, Randhir TO, Andayani N. Rhinos in the parks: an island-wide survey of the last wild population of the Sumatran rhinoceros. PLoS ONE. 2015; 10: e0139982. doi: 10.1371/journal.pone.0139982 26437186

48. Nagy-Reis MB, Nichols JD, Chiarello AG, Ribeiro MC, Setz EZF. Landscape use and co-occurrence patterns of Neotropical spotted cats. PLoS ONE. 2016; 12: e0168441.

49. Morato RG, Connette GM, Stabach JA, de Paula RC, Ferraz KMPM, Kantek DLZ, et al. Resource selection in an apex predator and variation in response to local landscape characteristics. Biol Conserv. 2018; 228: 233–240.

50. Alexander JS, Shi K, Tallents L, Riordan P. On the high trail: examining determinants of site use by the endangered snow leopard in Qilianshan, China. Oryx. 2016; 50: 231–238.

51. Hines JE. 2010. Program PRESENCE (Version 12.17). <http://www.mbr-pwrc.usgs.gov/software/doc/presence/presence.html>.

52. Rovero F, Zimmermann F, Berzi D, Meek P. “Which camera trap type and how many do I need?” A review of camera features and study designs for a range of wildlife research applications. Hystrix. 2013; 24: 148–156.

53. Olliff ERR, Cline CW, Bruen DC, Yarmchuk EJ, Pickles RSA, Hunter L. The Pantheracam–a camera trap optimized for monitoring wild felids. Wild Felid Monitor 2014; 7: 21–23.

54. Harmsen BJ, Foster RJ, Silver S, Ostro L, Doncaster CP. Differential use of trails by forest mammals and the implications for camera trap studies. Biotropica 2010; 42: 126–133.

55. Tobler MW, Zuñiga Hartley A, Carrillo-Percastegui SE, Powell GVN. 2015. Spatiotemporal hierarchical modelling of species richness and occupancy using camera trap data. J Appl Ecol. 2015; 52: 413–421.

56. Sollmann R, Furtado MM, Hofer H, Jácomo ATA, Torres NM, Silveira L. Using occupancy models to investigate space partitioning between two sympatric large predators, the jaguar and puma in central Brazil. Mamm Biol. 2012; 77: 41–46.

57. Figel JJ, Ruíz-Gutiérrez F, Brown DE. Densities and perceptions of jaguars in coastal Nayarit, Mexico. Wildl Soc Bull. 2016; 40: 506–513.

58. MacKenzie DI, Nichols JD, Lachman GB, Droege S, Royle JA, Langtimm CA. Estimating site occupancy rates when detection probabilities are less than one. Ecology. 2002; 83: 2248–2255.

59. MacKenzie DI, Nichols JD, Royle JA, Pollock KH, Bailey LL, Hines JE. Occupancy estimation and modeling: inferring patterns and dynamics of species occurrence. New York: Academic Press; 2006.

60. Burnham KP, Anderson DR. Model selection and multimodel inference: a practical information-theoretic approach. 2nd edn. New York: Springer-Verlag; 2002.

61. MacKenzie DI, Bailey LL. Assessing the fit of site-occupancy models. J Agric Biol Environ Stat. 2004; 9: 300–318.

62. MacKenzie DI, Nichols JD. Occupancy as a surrogate for abundance estimation. Anim Biodivers Conserv. 2004; 27: 461–467.

63. Crawshaw Jr PG, Quigley HB. Jaguar spacing, activity and habitat use in a seasonally flooded environment in Brazil. J Zool. 1991; 222: 357–370.

64. Zeller K, Nijhawan S, Salom-Pérez R, Potosme SH, Hines JE. Integrating occupancy modeling and interview data for corridor identification: a case study for jaguars in Nicaragua. Biol Conserv. 2011; 144: 892–901.

65. Cullen L Jr, Sana DA, Lima F, de Abreu KC, Uezu A. Selection of habitat by the jaguar in the upper Paraná river, Brazil. Zoologia. 2013; 30: 379–387.

66. Soisalo MK, Cavalcanti SMC. Estimating the density of a jaguar population in the Brazilian Pantanal using camera-traps and capture-recapture sampling in combination with GPS radio-telemetry. Biol Conserv. 2006; 129: 487–496.

67. Mekonnen MM, Hoekstra AY. The green, blue and grey water footprint of crops and derived crop products. Hydrol Earth Syst Sci. 2011; 15: 1577–1600.

68. Patino JE, Estupinan-Suarez LM. Hotspots of wetland area loss in Colombia. Wetlands. 2016; 36: 935–943.

69. Garcia-Ulloa J, Sloan S, Pacheco P, Ghazoul J, Koh LP. Lowering environmental costs of oil palm expansion in Colombia. Conserv Lett. 2012; 5: 366–375.

70. Ocampo-Peñuela N, Garcia-Ulloa J, Ghazoul J, Etter A. Quantifying impacts of oil palm expansion on Colombia’s threatened biodiversity. Biol Conserv. 2018; 224: 117–121.

71. IDEAM, IGAC, IAvH, Invemar, I Sinchi, IIAP. Ecosistemas continentales, costeros y marinos de Colombia. Bogotá: Instituto Geográfico Agustín Codazzi (IGAC); 2007.

72. Ramsar Convention Secretariat. The Ramsar Convention and its mission. Ramsar Conservation Secretariat, Gland, Switzerland. 2014.

73. Sanderson EJ, Forrest J, Loucks C, Ginsberg J, Dinerstein E, Seidensticker J, et al. Setting priorities for the conservation and recovery of wild tigers: 2005–2015. WCS, WWF, Smithsonian, NFWF-STF. New York–Washington DC. 2006.

74. Chanchani P, Noon BR, Bailey L, Warrier RA. Conserving tigers in working landscapes. Conserv Biol. 2016; 30: 649–660. doi: 10.1111/cobi.12633 26400445

75. Lamichhane BR, Leirs H, Persoon GA, Subedi N, Dhakal M, Oli BN, et al. Factors associated with co-occurrence of large carnivores in a human-dominated landscape. Biodiversity Conserv 2019; 28: 1473–1491.

76. Dobey S, Masters DV, Scheick BK, Clark JD, Pelton MR, Sunquist ME. Ecology of Florida black bears in the Okefenokee-Osceola ecosystem. Wildl Monogr. 2005; 158: 1–41.

77. Schaller GB, Vasconcelos JMC. Jaguar predation on capybara. Zeitschrift für Säugetierkunde. 1978; 43: 296–301.

78. Ramalho EE. Jaguar population dynamics, feeding ecology, human induced mortality, and conservation in the Varzea floodplain forests of Amazonia. PhD dissertation, University of Florida. 2012.

79. Bock BC, Páez VP, Daza JM. Trachemys callirostris (Gray 1856)–Colombian slider, jicotea, hicotea, galapago, morrocoy de agua. Chelonian Research Monographs. 2010; 5: 042.1–042.9.

80. Davidson NC, Finlayson CM. Extent, regional distribution and changes in area of different classes of wetland. Mar Freshwater Res. 2018; 69: 1525–1533.

81. Gumbricht T, Roman-Cuesta RM, Verchot L, Herold M, Wittmann F, Householder E, et al. An expert system model for mapping tropical wetlands and peatlands reveals South America as the largest contributor. Glob Change Biol. 2017; 23: 3581–3599.

82. Sasidhran S, Adila N, Hamdan MS, Samantha LD, Aziz N, Kamarudin N, et al. Habitat occupancy patterns and activity rate of native mammals in tropical fragmented peat swamp reserves in Peninsular Malaysia. Forest Ecol Manag. 2016; 363: 140–148.

83. Adila N, Sasidhran S, Kamarudin N, Puan CL, Azhar B, Lindenmayer DB. Effects of peat swamp logging and agricultural expansion on species richness of native mammals in Peninsular Malaysia. Basic Appl Ecol. 2017; 22: 1–10.

84. Jamhuri J, Samantha LD, Tee SL, Kamarudin N, Ashton-Butt A, Zubaid A, et al. Selective logging causes the decline of large-sized mammals including those in unlogged patches surrounded by logged and agricultural areas. Biol Conserv. 2018; 227: 40–47.

85. Locke A. The tigers of Terengganu. London, UK: Museum Press Ltd; 1954.

86. Khan MKM. Tiger in Malaysia: prospects for the future. In: Tilson RC, Seal US, editors. Tigers of the world. Park Ridge, New Jersey: Noyes Publications; 1987. p. 75–84.

87. Maddox T, Priatna D., Gemita E, Salampessy A. The conservation of tigers and other wildlife in oil palm plantations. London: Zoological Society of London; 2007.

88. Sunarto S, Kelly MJ, Parakkasi K, Klenzendorf S, Septayuda E, Kurniawan H. Tigers need cover: multi-scale occupancy study of the big cat in Sumatran forest and plantation landscapes. PLoS ONE. 2012; 7: e30859. doi: 10.1371/journal.pone.0030859 22292063

89. Alcrenaz M, Oram F, Ambu L, Lackman I, Ahmad E, Elahan H, et al. Of Pongo, palms and perceptions: a multidisciplinary assessment of Bornean orang-utans Pongo pygmaeus in an oil palm context. Oryx. 2015; 49: 465–472.

90. Sulai P, Nurhidayu S, Aziz N, Zakaria M, Barclary H, Azhar B. Effects of water quality in oil palm production landscapes on tropical waterbirds in Peninsular Malaysia. Ecol Res. 2015; 30: 941–949.

91. Karanth KU, Gopalaswamy AM, Kumar NS, Vaidyanathan S, Nichols JD, MacKenzie DI. Monitoring carnivore populations at the landscape scale: occupancy modelling of tigers from sign surveys. J Appl Ecol. 2011; 48: 1048–1056.

92. Hitchman SM, Mather ME, Smith JM, Fencl JS. Identifying keystone habitats with a mosaic approach can improve biodiversity conservation in disturbed ecosystems. Glob Change Biol. 2018; 24: 308–321.

93. Junk WJ, Piedade MTF, Schöngart J, Cohn-Haft M, Adeney JM, Wittmann F. A classification of major naturally-occurring Amazonian lowland wetlands. Wetlands. 2011; 31: 623–640.

94. Junk WJ. Current state of knowledge regarding South America wetlands and their future under global climate change. Aquat Sci. 2013; 75: 113–131.

95. Sica Y, Quintana R, Radeloff VC, Gavier-Pizarro G. Wetland loss due to land use change in the Lower Paraná River Delta, Argentina. Sci Total Environ. 2016; 568: 967–978. doi: 10.1016/j.scitotenv.2016.04.200 27369090

96. Rincón-Rubiano DR. Environmental Law in Colombia. 2nd ed. Alphen aan den Rijn: Kluwer Law International; 2011.


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