Habitat fragmentation, livelihood behaviors, and contact between people and nonhuman primates in Africa

Context Deforestation and landscape fragmentation have been identified as processes enabling direct transmission of zoonotic infections. Certain human behaviors provide opportunities for direct contact between humans and wild nonhuman primates (NHPs), but are often missing from studies linking landscape level factors and observed infectious diseases. Objectives Our objective is to better understand landscape and livelihood factors influencing human-NHP contact in rural communities whose landscapes undergo deforestation. We investigate core loss and edge density within a buffered area around survey respondent households to identify which landscape changes and behaviors increase the risk of human-NHP contact. Methods Behavioral survey data were collected from small-scale agriculturists living near forest fragments around Kibale National Park in western Uganda. We combined spatially explicit behavioral data with high-resolution satellite imagery. Using land cover classification and change detection, we investigated the relationships between forest loss and fragmentation, behavioral data, and human-NHP contact using logistic regression. Results Between 2011 and 2015, there were differences in the landscape metrics around the households of individuals who had experienced human-NHP contact compared to those who had not had contact. Increased edge density around households, collection of small trees for construction, and foraging and hunting for food in forested habitat significantly increase the likelihood of human-NHP contact. Conclusion This study provides empirical evidence that forest landscape fragmentation and certain smallholders’ behaviors in forest patches jointly increase the likelihood of human-NHP contact events. Combining spatially explicit data on land use and human behaviors is crucial for understanding the social and ecological drivers of human-NHP contact.

[1]  T. Struhsaker,et al.  Socioecology of Five Sympatric Monkey Species in the Kibale Forest, Uganda , 1979 .

[2]  T. Goldberg,et al.  Forest Fragmentation as Cause of Bacterial Transmission among Nonhuman Primates, Humans, and Livestock, Uganda , 2008, Emerging infectious diseases.

[3]  Oliver R. Wearn,et al.  Creation of forest edges has a global impact on forest vertebrates , 2017, Nature.

[4]  Ricard V. Solé,et al.  Habitat Fragmentation and Extinction Thresholds in Spatially Explicit Models , 1996 .

[5]  Charles M. Francis,et al.  Confronting collinearity: comparing methods for disentangling the effects of habitat loss and fragmentation , 2009, Landscape Ecology.

[6]  J. Hartter.  Resource Use and Ecosystem Services in a Forest Park Landscape , 2010 .

[7]  William B. Karesh,et al.  Habituating the great apes: the disease risks , 2002, Oryx.

[8]  R. Plowright,et al.  Null expectations for disease dynamics in shrinking habitat: dilution or amplification? , 2017, Philosophical Transactions of the Royal Society B: Biological Sciences.

[9]  T. Goldberg,et al.  Primates and the Ecology of their Infectious Diseases: How will Anthropogenic Change Affect Host‐Parasite Interactions? , 2005 .

[10]  Charles L. Nunn,et al.  Infectious Diseases in Primates , 2006 .

[11]  J. Bissonette,et al.  The behavior of landscape metrics commonly used in the study of habitat fragmentation , 1998, Landscape Ecology.

[12]  M. Herold,et al.  An assessment of deforestation and forest degradation drivers in developing countries , 2012 .

[13]  R. Ostfeld,et al.  Spatial epidemiology: an emerging (or re-emerging) discipline. , 2005, Trends in ecology & evolution.

[14]  Catrina A. Mackenzie.  Risk, Reciprocity and Retribution: Choosing to Extract Resources From a Protected Area , 2018 .

[15]  C. Chapman,et al.  Now there is no land: a story of ethnic migration in a protected area landscape in western Uganda , 2015 .

[16]  D. Ferber.  Human Diseases Threaten Great Apes , 2000, Science.

[17]  S. P. Henzi,et al.  Direction matching for sparse movement data sets: determining interaction rules in social groups , 2017 .

[18]  N. Wolfe,et al.  Coinfection of Ugandan Red Colobus (Procolobus [Piliocolobus] rufomitratus tephrosceles) with Novel, Divergent Delta-, Lenti-, and Spumaretroviruses , 2009, Journal of Virology.

[19]  David A. Wilkinson,et al.  Habitat fragmentation, biodiversity loss and the risk of novel infectious disease emergence , 2018, Journal of the Royal Society Interface.

[20]  R. Sengupta,et al.  Chasing baboons or attending class: protected areas and childhood education in Uganda , 2015, Environmental Conservation.

[21]  W. Heneine,et al.  Emergence of unique primate T-lymphotropic viruses among central African bushmeat hunters , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[22]  C. Hill,et al.  Crop Damage by Primates: Quantifying the Key Parameters of Crop-Raiding Events , 2012, PloS one.

[23]  Thomas Kenyon,et al.  Ebola 2014--new challenges, new global response and responsibility. , 2014, The New England journal of medicine.

[24]  S. Ryan,et al.  Household level influences on fragmentation in an African park landscape , 2015 .

[25]  Crop protection and conflict mitigation: reducing the costs of living alongside non-human primates , 2012, Biodiversity and Conservation.

[26]  Jay R. Malcolm,et al.  Edge effects in central Amazonian forest fragments , 1994 .

[27]  Colin A. Chapman,et al.  Analysing small-scale aggregation in animal visits in space and time: the ST-BBD method , 2013, Animal Behaviour.

[28]  C. Chapman,et al.  Long‐Term Effects of Logging on African Primate Communities: a 28‐Year Comparison From Kibale National Park, Uganda , 2000 .

[29]  Daphne A. Onderdonk,et al.  Coping with Forest Fragmentation: The Primates of Kibale National Park, Uganda , 2000, International Journal of Primatology.

[30]  K. Brandon,et al.  The role of protected areas in conserving biodiversity and sustaining local livelihoods , 2005 .

[31]  S. Strum.  The Development of Primate Raiding: Implications for Management and Conservation , 2010, International Journal of Primatology.

[32]  Charles L. Nunn,et al.  Infectious diseases in primates: behavior, ecology and evolution. , 2006 .

[33]  J. Jones,et al.  Beyond Bushmeat: Animal Contact, Injury, and Zoonotic Disease Risk in Western Uganda , 2014, EcoHealth.

[34]  L. Naughton-Treves.  Predicting Patterns of Crop Damage by Wildlife around Kibale National Park, Uganda , 1998 .

[35]  D. Bausch,et al.  Outbreak of Ebola Virus Disease in Guinea: Where Ecology Meets Economy , 2014, PLoS neglected tropical diseases.

[36]  Catherine Linard,et al.  Assessing the use of global land cover data for guiding large area population distribution modelling , 2010, GeoJournal.

[37]  C. Chapman,et al.  Habitat alteration and the conservation of African primates: Case study of Kibale National Park, Uganda , 2000, American journal of primatology.

[38]  Chris Cosner,et al.  How Habitat Edges Change Species Interactions , 1999, The American Naturalist.

[39]  J. Southworth,et al.  Dwindling resources and fragmentation of landscapes around parks: wetlands and forest patches around Kibale National Park, Uganda , 2009, Landscape Ecology.

[40]  J. Obua,et al.  Patterns of crop raiding by primates around the Budongo Forest Reserve, Uganda , 2005 .

[41]  Wilfried Thuiller,et al.  Comparing species interaction networks along environmental gradients , 2017, Biological reviews of the Cambridge Philosophical Society.

[42]  C. Nunn,et al.  Emerging infectious diseases and animal social systems , 2008, Evolutionary Ecology.

[43]  C. Hill.  Perspectives of “Conflict” at the Wildlife–Agriculture Boundary: 10 Years On , 2015 .

[44]  R. Cristescu,et al.  How Ebola impacts social dynamics in gorillas: a multistate modelling approach. , 2015, The Journal of animal ecology.

[45]  T. Clutton‐Brock.  Ranging behaviour of red colobus (Colobus badius tephrosceles) in the Gombe National Park , 1975, Animal Behaviour.

[46]  L. Fahrig.  Effects of Habitat Fragmentation on Biodiversity , 2003 .

[47]  C. Chapman,et al.  Spatial patterns of illegal resource extraction in Kibale National Park, Uganda , 2011, Environmental Conservation.

[48]  T. Goldberg,et al.  Spatial configuration becomes more important with increasing habitat loss: a simulation study of environmentally-transmitted parasites , 2018, Landscape Ecology.

[49]  W. Zipperer.  Deforestation patterns and their effects on forest patches , 1993, Landscape Ecology.

[50]  R. Didham,et al.  Using landscape history to predict biodiversity patterns in fragmented landscapes , 2013, Ecology letters.

[51]  R. Plowright,et al.  Pathogen spillover during land conversion. , 2018, Ecology letters.

[52]  Niko Speybroeck,et al.  Consequences of Landscape Fragmentation on Lyme Disease Risk: A Cellular Automata Approach , 2012, PloS one.

[53]  A. Fuentes,et al.  A test of agent-based models as a tool for predicting patterns of pathogen transmission in complex landscapes , 2013, BMC Ecology.

[54]  Catrina A. Mackenzie,et al.  Elephants in the garden: Financial and social costs of crop raiding , 2012 .

[55]  J. Hartter,et al.  Demand and proximity: drivers of illegal forest resource extraction , 2013, Oryx.

[56]  R. Forman.  Some general principles of landscape and regional ecology , 1995, Landscape Ecology.

[57]  W. Laurance,et al.  Impacts of roads and linear clearings on tropical forests. , 2009, Trends in ecology & evolution.

[58]  Philip M Clarke,et al.  Optimal recall length in survey design. , 2008, Journal of health economics.

[59]  C. Hill.  Farmers’ Perspectives of Conflict at the Wildlife–Agriculture Boundary: Some Lessons Learned from African Subsistence Farmers , 2004 .

[60]  L. Naughton-Treves.  FARMING THE FOREST EDGE: VULNERABLE PLACES AND PEOPLE AROUND KIBALE NATIONAL PARK, UGANDA , 1997 .

[61]  J. Pépin.  The Origins of AIDS , 2011 .

[62]  C. Tucker,et al.  Tropical Deforestation and Habitat Fragmentation in the Amazon: Satellite Data from 1978 to 1988 , 1993, Science.

[63]  C. Chapman,et al.  Parks, People and Pixels: Evaluating Landscape Effects of an East African National Park on its Surroundings , 2010 .

[64]  G. Bonanno,et al.  Retrospective memory bias for the frequency of potentially traumatic events: A prospective study. , 2011 .

[65]  C. Chapman,et al.  Forest Restoration in Abandoned Agricultural Land: a Case Study from East Africa , 1999 .

[66]  Rosie Woodroffe,et al.  People and Wildlife, Conflict or Co-existence? , 2005 .

[67]  E. Kakudidi.  A study of plant materials used for house construction around Kibale National Park, western Uganda , 2007 .

[68]  K. McGarigal,et al.  FRAGSTATS: spatial pattern analysis program for quantifying landscape structure. , 1995 .

[69]  A. McMichael,et al.  Ecosystems and Human well-being , 2003 .

[70]  Thomas M. Butynski,et al.  Comparative Ecology of Blue Monkeys (Cercopithecus Mitis) in High‐ and Low‐Density Subpopulations , 1990 .

[71]  J. Gonzalez,et al.  Ebola virus circulation in Africa: a balance between clinical expression and epidemiological silence. , 2005, Bulletin de la Societe de pathologie exotique.

[72]  Belinda A. Margono,et al.  Mapping and monitoring deforestation and forest degradation in Sumatra (Indonesia) using Landsat time series data sets from 1990 to 2010 , 2012 .

[73]  Robert Nasi,et al.  Recent loss of closed forests is associated with Ebola virus disease outbreaks , 2017, Scientific Reports.

[74]  L. Wolfe,et al.  Commensalism and conflict : the human-primate interface , 2005 .

[75]  Ahindra Ghosh,et al.  Ecosystems and Human Well-Being , 2013 .

[76]  C. Chapman,et al.  Censusing large mammals in Kibale National Park: evaluation of the intensity of sampling required to determine change , 2010 .