Anthropogenic disturbance favours generalist over specialist parasites in bird communities: Implications for risk of disease emergence

Dharmarajan, Guha; Gupta, Pooja; Vishnudas, C. K.; Robin, V. V.; Ostfeld, ed., Richard

doi:10.1111/ele.13818

Title: Anthropogenic disturbance favours generalist over specialist parasites in bird communities: Implications for risk of disease emergence

Journal Article · 12 June 2021 · Ecology Letters

DOI: https://doi.org/10.1111/ele.13818 · OSTI ID:1788121

^[1];

^[1]; Vishnudas, C. K. ^[2];

^[2]; Ostfeld, ed., Richard

Savannah River Ecology Laboratory University of Georgia Aiken SC USA, Indian Institute of Science Education and Research Kolkata Mohanpur West Bengal India
Indian Institute of Science Education and Research Tirupati Tirupati Andhra Pradesh India

Abstract Niche theory predicts specialists which will be more sensitive to environmental perturbation compared to generalists, a hypothesis receiving broad support in free‐living species. Based on their niche breadth, parasites can also be classified as specialists and generalists, with specialists infecting only a few and generalists a diverse array of host species. Here, using avian haemosporidian parasites infecting wild bird populations inhabiting the Western Ghats, India as a model system, we elucidate how climate, habitat and human disturbance affects parasite prevalence both directly and indirectly via their effects on host diversity. Our data demonstrate that anthropogenic disturbance acts to reduce the prevalence of specialist parasite lineages, while increasing that of generalist lineages. Thus, as in free‐living species, disturbance favours parasite communities dominated by generalist versus specialist species. Because generalist parasites are more likely to cause emerging infectious diseases, such biotic homogenisation of parasite communities could increase disease emergence risk in the Anthropocene.

View Accepted Manuscript (Publisher)

Cite

Export

Save

Sponsoring Organization:: USDOE

Grant/Contract Number:: EM0004391

OSTI ID:: 1788121

Journal Information:: Ecology Letters, Journal Name: Ecology Letters Journal Issue: 9 Vol. 24; ISSN 1461-023X

Publisher:: Wiley-BlackwellCopyright Statement

Country of Publication:: United Kingdom

Language:: English

References (78)

Is biodiversity bad for your health? Ostfeld, Richard S.; Keesing, Felicia Ecosphere, Vol. 8, Issue 3 https://doi.org/10.1002/ecs2.1676	journal	March 2017
Towards a more healthy conservation paradigm: integrating disease and molecular ecology to aid biological conservation† Gupta, Pooja; Robin, V. V.; Dharmarajan, Guha Journal of Genetics, Vol. 99, Issue 1 https://doi.org/10.1007/s12041-020-01225-7	journal	July 2020
What makes a specialist special? Timms, Rebecca; Read, Andrew F. Trends in Ecology & Evolution, Vol. 14, Issue 9 https://doi.org/10.1016/S0169-5347(99)01697-3	journal	September 1999
Effects of landscape anthropization on sylvatic mosquito assemblages in a rainforest in Chiapas, Mexico Orta-Pineda, Guillermo; Abella-Medrano, Carlos Antonio; Suzán, Gerardo Acta Tropica, Vol. 216 https://doi.org/10.1016/j.actatropica.2021.105849	journal	April 2021
Resource use and rarity among frugivorous birds in a tropical rain forest on Sulawesi Walker, Jonathan S. Biological Conservation, Vol. 130, Issue 1 https://doi.org/10.1016/j.biocon.2005.12.002	journal	June 2006
Distribution patterns, range size and niche breadth of Austrian endemic plants Essl, Franz; Staudinger, Markus; Stöhr, Oliver Biological Conservation, Vol. 142, Issue 11 https://doi.org/10.1016/j.biocon.2009.05.027	journal	November 2009
Taxonomic, phylogenetic and functional homogenization of bird communities due to land use change Liang, Chenxia; Yang, Guisheng; Wang, Na Biological Conservation, Vol. 236 https://doi.org/10.1016/j.biocon.2019.05.036	journal	August 2019
When the winners are the losers: Invasive alien bird species outcompete the native winners in the biotic homogenization process Colléony, Agathe; Shwartz, Assaf Biological Conservation, Vol. 241 https://doi.org/10.1016/j.biocon.2019.108314	journal	January 2020
Incorporating coextinction in threat assessments and policy will rapidly improve the accuracy of threatened species lists Moir, Melinda L.; Brennan, Karl E. C. Biological Conservation, Vol. 249 https://doi.org/10.1016/j.biocon.2020.108715	journal	September 2020
Extinction in the Anthropocene Turvey, Samuel T.; Crees, Jennifer J. Current Biology, Vol. 29, Issue 19 https://doi.org/10.1016/j.cub.2019.07.040	journal	October 2019
The Anthropocene Laurance, William F. Current Biology, Vol. 29, Issue 19 https://doi.org/10.1016/j.cub.2019.07.055	journal	October 2019
Neglected wild life: Parasitic biodiversity as a conservation target Gómez, Andrés; Nichols, Elizabeth International Journal for Parasitology: Parasites and Wildlife, Vol. 2 https://doi.org/10.1016/j.ijppaw.2013.07.002	journal	December 2013
New vegetation type map of India prepared using satellite remote sensing: Comparison with global vegetation maps and utilities Roy, P. S.; Behera, M. D.; Murthy, M. S. R. International Journal of Applied Earth Observation and Geoinformation, Vol. 39 https://doi.org/10.1016/j.jag.2015.03.003	journal	July 2015
Parasites at Risk – Insights from an Endangered Marsupial Thompson, R. C. Andrew; Lymbery, Alan J.; Godfrey, Stephanie S. Trends in Parasitology, Vol. 34, Issue 1 https://doi.org/10.1016/j.pt.2017.09.001	journal	January 2018
Host Specificity in Variable Environments Wells, Konstans; Clark, Nicholas J. Trends in Parasitology, Vol. 35, Issue 6 https://doi.org/10.1016/j.pt.2019.04.001	journal	June 2019
Is a healthy ecosystem one that is rich in parasites? Hudson, Peter J.; Dobson, Andrew P.; Lafferty, Kevin D. Trends in Ecology & Evolution, Vol. 21, Issue 7 https://doi.org/10.1016/j.tree.2006.04.007	journal	July 2006
The Anthropocene concept in ecology and conservation Corlett, Richard T. Trends in Ecology & Evolution, Vol. 30, Issue 1 https://doi.org/10.1016/j.tree.2014.10.007	journal	January 2015
Role of human population size in raising bird and mammal threat among nations McKinney, Michael L. Animal Conservation, Vol. 4, Issue 1 https://doi.org/10.1017/S1367943001001056	journal	February 2001
Species that can make us ill thrive in human habitats Ostfeld, Richard S.; Keesing, Felicia Nature, Vol. 584, Issue 7821 https://doi.org/10.1038/d41586-020-02189-5	journal	August 2020
Biodiversity decreases disease through predictable changes in host community competence Johnson, Pieter T. J.; Preston, Daniel L.; Hoverman, Jason T. Nature, Vol. 494, Issue 7436 https://doi.org/10.1038/nature11883	journal	February 2013
Global hotspots and correlates of emerging zoonotic diseases Allen, Toph; Murray, Kris A.; Zambrana-Torrelio, Carlos Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-00923-8	journal	October 2017
Adaptive responses of animals to climate change are most likely insufficient Radchuk, Viktoriia; Reed, Thomas; Teplitsky, Céline Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-10924-4	journal	July 2019
Zoonotic host diversity increases in human-dominated ecosystems Gibb, Rory; Redding, David W.; Chin, Kai Qing Nature, Vol. 584, Issue 7821 https://doi.org/10.1038/s41586-020-2562-8	journal	August 2020
Disturbance and mosquito diversity in the lowland tropical rainforest of central Panama Loaiza, Jose R.; Dutari, Larissa C.; Rovira, Jose R. Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-07476-2	journal	August 2017
Co-extinctions annihilate planetary life during extreme environmental change Strona, Giovanni; Bradshaw, Corey J. A. Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-35068-1	journal	November 2018
Responses of ‘resistant’ vertebrates to habitat loss and fragmentation: the importance of niche breadth and range boundaries Swihart, Robert K.; Gehring, Thomas M.; Kolozsvary, Mary Beth Diversity and Distributions, Vol. 9, Issue 1 https://doi.org/10.1046/j.1472-4642.2003.00158.x	journal	December 2002
Predicting the risk of extinction from shared ecological characteristics Kotiaho, J. S.; Kaitala, V.; Komonen, A. Proceedings of the National Academy of Sciences, Vol. 102, Issue 6 https://doi.org/10.1073/pnas.0406718102	journal	January 2005
Homage to Linnaeus: How many parasites? How many hosts? Dobson, A.; Lafferty, K. D.; Kuris, A. M. Proceedings of the National Academy of Sciences, Vol. 105, Issue Supplement 1 https://doi.org/10.1073/pnas.0803232105	journal	August 2008
Biodiversity enhances reef fish biomass and resistance to climate change Duffy, J. Emmett; Lefcheck, Jonathan S.; Stuart-Smith, Rick D. Proceedings of the National Academy of Sciences, Vol. 113, Issue 22 https://doi.org/10.1073/pnas.1524465113	journal	May 2016
Host Specialization and Geographic Localization of Avian Malaria Parasites: A Regional Analysis in the Lesser Antilles Fallon, Sylvia M.; Bermingham, Eldredge; Ricklefs, Robert E. The American Naturalist, Vol. 165, Issue 4 https://doi.org/10.1086/428430	journal	April 2005
The study of parasite sharing for surveillance of zoonotic diseases Farrell, Maxwell J.; Berrang-Ford, Lea; Davies, T. Jonathan Environmental Research Letters, Vol. 8, Issue 1 https://doi.org/10.1088/1748-9326/8/1/015036	journal	March 2013
Niche breadth and geographical range: ecological compensation for geographical rarity in rainforest frogs Williams, Yvette M.; Williams, Stephen E.; Alford, Ross A. Biology Letters, Vol. 2, Issue 4 https://doi.org/10.1098/rsbl.2006.0541	journal	September 2006
Brain size and resource specialization predict long-term population trends in British birds Shultz, Susanne; B. Bradbury, Richard; L. Evans, Karl Proceedings of the Royal Society B: Biological Sciences, Vol. 272, Issue 1578 https://doi.org/10.1098/rspb.2005.3250	journal	September 2005
The sixth mass coextinction: are most endangered species parasites and mutualists? Dunn, Robert R.; Harris, Nyeema C.; Colwell, Robert K. Proceedings of the Royal Society B: Biological Sciences, Vol. 276, Issue 1670 https://doi.org/10.1098/rspb.2009.0413	journal	May 2009
Geographical and host species barriers differentially affect generalist and specialist parasite community structure in a tropical sky-island archipelago Gupta, Pooja; Vishnudas, C. K.; Ramakrishnan, Uma Proceedings of the Royal Society B: Biological Sciences, Vol. 286, Issue 1904 https://doi.org/10.1098/rspb.2019.0439	journal	June 2019
Changes in taxonomic and phylogenetic diversity in the Anthropocene Li, Daijiang; Olden, Julian D.; Lockwood, Julie L. Proceedings of the Royal Society B: Biological Sciences, Vol. 287, Issue 1929 https://doi.org/10.1098/rspb.2020.0777	journal	June 2020
BAT – Biodiversity Assessment Tools, an R package for the measurement and estimation of alpha and beta taxon, phylogenetic and functional diversity Cardoso, Pedro; Rigal, François; Carvalho, José C. Methods in Ecology and Evolution, Vol. 6, Issue 2 https://doi.org/10.1111/2041-210X.12310	journal	December 2014
piecewiseSEM : Piecewise structural equation modelling in r for ecology, evolution, and systematics Lefcheck, Jonathan S. Methods in Ecology and Evolution, Vol. 7, Issue 5 https://doi.org/10.1111/2041-210X.12512	journal	December 2015
Ecological and evolutionary legacy of megafauna extinctions: Anachronisms and megafauna interactions Galetti, Mauro; Moleón, Marcos; Jordano, Pedro Biological Reviews, Vol. 93, Issue 2 https://doi.org/10.1111/brv.12374	journal	October 2017
Paradigms for parasite conservation: Parasite Conservation Dougherty, Eric R.; Carlson, Colin J.; Bueno, Veronica M. Conservation Biology, Vol. 30, Issue 4 https://doi.org/10.1111/cobi.12634	journal	December 2015
Niche breadth predicts geographical range size: a general ecological pattern Slatyer, Rachel A.; Hirst, Megan; Sexton, Jason P. Ecology Letters, Vol. 16, Issue 8 https://doi.org/10.1111/ele.12140	journal	June 2013
Frontiers in research on biodiversity and disease Johnson, Pieter T. J.; Ostfeld, Richard S.; Keesing, Felicia Ecology Letters, Vol. 18, Issue 10 https://doi.org/10.1111/ele.12479	journal	August 2015
Niche breadth and geographic range size as determinants of species survival on geological time scales: Determinants of species survival Saupe, Erin E.; Qiao, Huijie; Hendricks, Jonathan R. Global Ecology and Biogeography, Vol. 24, Issue 10 https://doi.org/10.1111/geb.12333	journal	June 2015
Disease emergence and invasions Hatcher, Melanie J.; Dick, Jaimie T. A.; Dunn, Alison M. Functional Ecology, Vol. 26, Issue 6 https://doi.org/10.1111/j.1365-2435.2012.02031.x	journal	July 2012
Biotic homogenization: a new research agenda for conservation biogeography Olden, Julian D. Journal of Biogeography, Vol. 33, Issue 12 https://doi.org/10.1111/j.1365-2699.2006.01572.x	journal	December 2006
Host and habitat specialization of avian malaria in Africa: HOST AND HABITAT SPECIALIZATION OF AVIAN MALARIA Loiseau, Claire; Harrigan, Ryan J.; Robert, Alexandre Molecular Ecology, Vol. 21, Issue 2 https://doi.org/10.1111/j.1365-294X.2011.05341.x	journal	December 2011
Are specialists at risk under environmental change? Neoecological, paleoecological and phylogenetic approaches Colles, Audrey; Liow, Lee Hsiang; Prinzing, Andreas Ecology Letters, Vol. 12, Issue 8 https://doi.org/10.1111/j.1461-0248.2009.01336.x	journal	August 2009
Establishment of exotic parasites: the origins and characteristics of an avian malaria community in an isolated island avifauna Ewen, John G.; Bensch, Staffan; Blackburn, Tim M. Ecology Letters, Vol. 15, Issue 10 https://doi.org/10.1111/j.1461-0248.2012.01833.x	journal	July 2012
Phylogenetic host specificity and understanding parasite sharing in primates Cooper, Natalie; Griffin, Randi; Franz, Mathias Ecology Letters, Vol. 15, Issue 12 https://doi.org/10.1111/j.1461-0248.2012.01858.x	journal	August 2012
On defining and quantifying biotic homogenization: Defining biotic homogenization Olden, Julian D.; Rooney, Thomas P. Global Ecology and Biogeography, Vol. 15, Issue 2 https://doi.org/10.1111/j.1466-822X.2006.00214.x	journal	February 2006
A Comparative Analysis of Specialization and Extinction Risk in Temperate-Zone Bats Safi, Kamran; Kerth, Gerald Conservation Biology, Vol. 18, Issue 5 https://doi.org/10.1111/j.1523-1739.2004.00155.x	journal	October 2004
The phylogenetic range of bacterial and viral pathogens of vertebrates Shaw, Liam P.; Wang, Alethea D.; Dylus, David Molecular Ecology, Vol. 29, Issue 17 https://doi.org/10.1111/mec.15463	journal	June 2020
Evolutionary responses to global change in species‐rich communities Lau, Jennifer A.; terHorst, Casey P. Annals of the New York Academy of Sciences, Vol. 1476, Issue 1 https://doi.org/10.1111/nyas.14221	journal	August 2019
Forest disturbance and vector transmitted diseases in the lowland tropical rainforest of central Panama Loaiza, Jose R.; Rovira, Jose R.; Sanjur, Oris I. Tropical Medicine & International Health, Vol. 24, Issue 7 https://doi.org/10.1111/tmi.13244	journal	May 2019
Population Biology of Multihost Pathogens Woolhouse, M. E. J. Science, Vol. 292, Issue 5519 https://doi.org/10.1126/science.1059026	journal	May 2001
Species Coextinctions and the Biodiversity Crisis Koh, L. P. Science, Vol. 305, Issue 5690 https://doi.org/10.1126/science.1101101	journal	September 2004
Fundamental Evolutionary Limits in Ecological Traits Drive Drosophila Species Distributions Kellermann, V.; van Heerwaarden, B.; Sgro, C. M. Science, Vol. 325, Issue 5945 https://doi.org/10.1126/science.1175443	journal	September 2009
Defaunation in the Anthropocene Dirzo, R.; Young, H. S.; Galetti, M. Science, Vol. 345, Issue 6195 https://doi.org/10.1126/science.1251817	journal	July 2014
Why infectious disease research needs community ecology Johnson, P. T. J.; de Roode, J. C.; Fenton, A. Science, Vol. 349, Issue 6252 https://doi.org/10.1126/science.1259504	journal	September 2015
Effects of Host Diversity on Infectious Disease Ostfeld, Richard S.; Keesing, Felicia Annual Review of Ecology, Evolution, and Systematics, Vol. 43, Issue 1 https://doi.org/10.1146/annurev-ecolsys-102710-145022	journal	December 2012
Coextinction and Persistence of Dependent Species in a Changing World Colwell, Robert K.; Dunn, Robert R.; Harris, Nyeema C. Annual Review of Ecology, Evolution, and Systematics, Vol. 43, Issue 1 https://doi.org/10.1146/annurev-ecolsys-110411-160304	journal	December 2012
Patterns, Causes, and Consequences of Anthropocene Defaunation Young, Hillary S.; McCauley, Douglas J.; Galetti, Mauro Annual Review of Ecology, Evolution, and Systematics, Vol. 47, Issue 1 https://doi.org/10.1146/annurev-ecolsys-112414-054142	journal	November 2016
Host phylogeny matters: Examining sources of variation in infection risk by blood parasites across a tropical montane bird community in India Gupta, Pooja; Vishnudas, C. K.; Robin, V. V. Parasites & Vectors, Vol. 13, Issue 1 https://doi.org/10.1186/s13071-020-04404-8	journal	October 2020
Diversity, decoys and the dilution effect: how ecological communities affect disease risk Johnson, P. T. J.; Thieltges, D. W. Journal of Experimental Biology, Vol. 213, Issue 6 https://doi.org/10.1242/jeb.037721	journal	February 2010
Biodiversity Can Help Prevent Malaria Outbreaks in Tropical Forests Laporta, Gabriel Zorello; Prado, Paulo Inácio Knegt Lopez de; Kraenkel, Roberto André PLoS Neglected Tropical Diseases, Vol. 7, Issue 3 https://doi.org/10.1371/journal.pntd.0002139	journal	March 2013
The Perils of Picky Eating: Dietary Breadth Is Related to Extinction Risk in Insectivorous Bats Boyles, Justin G.; Storm, Jonathan J. PLoS ONE, Vol. 2, Issue 7 https://doi.org/10.1371/journal.pone.0000672	journal	July 2007
Elevational Distribution and Extinction Risk in Birds White, Rachel L.; Bennett, Peter M. PLOS ONE, Vol. 10, Issue 4 https://doi.org/10.1371/journal.pone.0121849	journal	April 2015
Is Avian Malaria Playing a Role in Native Bird Declines in New Zealand? Testing Hypotheses along an Elevational Gradient Niebuhr, Chris N.; Poulin, Robert; Tompkins, Daniel M. PLOS ONE, Vol. 11, Issue 11 https://doi.org/10.1371/journal.pone.0165918	journal	November 2016
Effect of land-use changes on the abundance, distribution, and host-seeking behavior of Aedes arbovirus vectors in oil palm-dominated landscapes, southeastern Côte d’Ivoire Zahouli, Julien B. Z.; Koudou, Benjamin G.; Müller, Pie PLOS ONE, Vol. 12, Issue 12 https://doi.org/10.1371/journal.pone.0189082	journal	December 2017
Building Predictive Models in R Using the caret Package Kuhn, Max Journal of Statistical Software, Vol. 28, Issue 5 https://doi.org/10.18637/jss.v028.i05	journal	January 2008
ranger : A Fast Implementation of Random Forests for High Dimensional Data in C++ and R Wright, Marvin N.; Ziegler, Andreas Journal of Statistical Software, Vol. 77, Issue 1 https://doi.org/10.18637/jss.v077.i01	journal	January 2017
Worldwide decline of specialist species: toward a global functional homogenization? Clavel, Joanne; Julliard, Romain; Devictor, Vincent Frontiers in Ecology and the Environment, Vol. 9, Issue 4 https://doi.org/10.1890/080216	journal	June 2010
The AIC model selection method applied to path analytic models compared using a d-separation test Shipley, Bill Ecology, Vol. 94, Issue 3 https://doi.org/10.1890/12-0976.1	journal	March 2013
The Role of Introduced Diseases in the Extinction of the Endemic Hawaiian Avifauna Warner, Richard E. The Condor, Vol. 70, Issue 2 https://doi.org/10.2307/1365954	journal	April 1968
Deforestation and Malaria in Mâncio Lima County, Brazil Olson, Sarah H.; Gangnon, Ronald; Silveira, Guilherme Abbad Emerging Infectious Diseases, Vol. 16, Issue 7 https://doi.org/10.3201/eid1607.091785	journal	July 2010
Visualization of Regression Models Using visreg Breheny, Patrick; Burchett, Woodrow The R Journal, Vol. 9, Issue 2 https://doi.org/10.32614/RJ-2017-046	journal	January 2017
Land Use Influences Mosquito Communities and Disease Risk on Remote Tropical Islands: A Case Study Using a Novel Sampling Technique Laurance, Susan G. W.; Meyer Steiger, Dagmar B.; Ritchie, Scott Alex The American Journal of Tropical Medicine and Hygiene, Vol. 94, Issue 2 https://doi.org/10.4269/ajtmh.15-0161	journal	February 2016
Impact of Deforestation and Agricultural Development on Anopheline Ecology and Malaria Epidemiology Levins, Richard; Yasuoka, Junko The American Journal of Tropical Medicine and Hygiene, Vol. 76, Issue 3 https://doi.org/10.4269/ajtmh.2007.76.450	journal	March 2007

Similar Records

Host phylogeny matters: Examining sources of variation in infection risk by blood parasites across a tropical montane bird community in India

Journal Article · 2020 · Parasites & Vectors · OSTI ID:1690316

Gupta, Pooja; Vishnudas, C. K.; Robin, V. V.; +1 more

Geographical and host species barriers differentially affect generalist and specialist parasite community structure in a tropical sky-island archipelago

Journal Article · 2019 · Proceedings of the Royal Society B: Biological Sciences · OSTI ID:1819706

Gupta, Pooja; Vishnudas, C. K.; Ramakrishnan, Uma; +2 more

Global drivers of avian haemosporidian infections vary across zoogeographical regions

Journal Article · 2021 · Global Ecology and Biogeography · OSTI ID:1980622

Fecchio, Alan; Clark, Nicholas J.; Bell, Jeffrey A.; +38 more

Title: Anthropogenic disturbance favours generalist over specialist parasites in bird communities: Implications for risk of disease emergence

Citation Formats

References (78)

Similar Records

Related Subjects