Award Abstract # 1754171
NSFDEB-NERC: Diversity and disease: uniting community and disease ecology to understand how biodiversity affects parasite transmission

NSF Org: DEB
Division Of Environmental Biology
Recipient: THE REGENTS OF THE UNIVERSITY OF COLORADO
Initial Amendment Date: July 10, 2018
Latest Amendment Date: February 27, 2023
Award Number: 1754171
Award Instrument: Standard Grant
Program Manager: Steven Dudgeon
sdudgeon@nsf.gov
 (703)292-2279
DEB
 Division Of Environmental Biology
BIO
 Directorate for Biological Sciences
Start Date: July 15, 2018
End Date: December 31, 2024 (Estimated)
Total Intended Award Amount: $604,947.00
Total Awarded Amount to Date: $719,334.00
Funds Obligated to Date: FY 2018 = $604,947.00
FY 2019 = $6,250.00

FY 2020 = $35,952.00

FY 2021 = $49,755.00

FY 2022 = $14,430.00

FY 2023 = $8,000.00
History of Investigator:
  • Pieter Johnson (Principal Investigator)
    pieter.johnson@colorado.edu
  • Andy Fenton (Co-Principal Investigator)
Recipient Sponsored Research Office: University of Colorado at Boulder
3100 MARINE ST
Boulder
CO  US  80309-0001
(303)492-6221
Sponsor Congressional District: 02
Primary Place of Performance: University of Colorado at Boulder
3100 Marine Street, Room 481
Boulder
CO  US  80303-1058
Primary Place of Performance
Congressional District:
02
Unique Entity Identifier (UEI): SPVKK1RC2MZ3
Parent UEI:
NSF Program(s): Evolutionary Processes,
Population & Community Ecology,
POP & COMMUNITY ECOL PROG
Primary Program Source: 01002324DB NSF RESEARCH & RELATED ACTIVIT
01001819DB NSF RESEARCH & RELATED ACTIVIT

01001920DB NSF RESEARCH & RELATED ACTIVIT

01002021DB NSF RESEARCH & RELATED ACTIVIT

01002122DB NSF RESEARCH & RELATED ACTIVIT

01002223DB NSF RESEARCH & RELATED ACTIVIT
Program Reference Code(s): 108Z, 7744, 1182, 9251, 019Z, 102Z
Program Element Code(s): 112700, 112800, 118200
Award Agency Code: 4900
Fund Agency Code: 4900
Assistance Listing Number(s): 47.074

ABSTRACT

Over the next century, two of the most pressing environmental threats will be the ongoing losses of biodiversity and the increased emergence of infectious diseases. Key challenges are to understand how these issues are related and to identify strategies for reducing their effects on human and wildlife populations. For instance, growing evidence suggests that the diversity of organisms found in natural habitats can affect how fast pathogens spread, including those that cause illness in humans. This research will investigate how changes in species diversity affect the risk of infection and disease in a threatened group of wildlife: amphibians. Researchers from the USA and the United Kingdom will work together to better understand how diversity influences pathogen transmission, using mechanistic models of infection fit to data from field observations, laboratory experiments, and whole-system manipulations. Results of the research will be used to assist natural resource managers to conserve threatened amphibian populations and to develop an interactive exhibit at the University of Colorado Natural History Museum which will engage elementary and middle school students. The project will also provide opportunities for broadening participation in science by involving undergraduate and graduate students.

This proposal applies tools and concepts from community ecology to test the foundational relationships between biological diversity and parasite infection. Building upon extensive previous research by the investigators, data from (i) wetland surveys will be used to understand how communities of amphibians (frogs, toads, and salamanders) and infectious parasites change along a gradient in biodiversity. Field data will be combined with results from (ii) laboratory experiments that test alternative mechanisms through which biodiversity might affect infections to develop (iii) predictive models that forecast the influence of each mechanism on disease risk. Finally, model predictions will be tested and refined using a (iv) real-world experiment in which the presence and abundance of an influential host species is altered across a natural richness gradient. Results will be compared among parasite species that differ in the amount of disease they cause in amphibian hosts. The integration of wetland surveys, multi-scale experiments, and predictive modeling will fill a key knowledge gap by assessing the functional relationships between biodiversity and parasite transmission, which are difficult to discern from strictly observational data or studies of a single host or parasite species. These efforts will help resolve ongoing debates about the diversity-disease relationship and build a more comprehensive understanding of how changes in ecological communities interact to influence disease risk.

This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.

PUBLICATIONS PRODUCED AS A RESULT OF THIS RESEARCH

Note:  When clicking on a Digital Object Identifier (DOI) number, you will be taken to an external site maintained by the publisher. Some full text articles may not yet be available without a charge during the embargo (administrative interval).

Some links on this page may take you to non-federal websites. Their policies may differ from this site.

(Showing: 1 - 10 of 28)
Johnson, Pieter T.J. and Calhoun, Dana M. and Riepe, Tawni B. and Koprivnikar, Janet "Chance or choice? Understanding parasite selection and infection in multi-host communities" International Journal for Parasitology , v.49 , 2019 10.1016/j.ijpara.2018.12.007 Citation Details
Calhoun, Dana M. and Curtis, Jamie and Hassan, Clara and Johnson, Pieter T. "Putting infection on the map: Using heatmaps to characterize within- and between-host distributions of trematode metacercariae" Journal of Helminthology , v.97 , 2023 https://doi.org/10.1017/S0022149X2300069X Citation Details
Calhoun, Dana M. and Esfahani, Evan and Locke, Sean A. and Moser, William E. and Johnson, Pieter T.J. "How parasite exposure and time interact to determine Australapatemon burti (Trematoda: Digenea) infections in second intermediate hosts (Erpobdella microstoma) (Hirudinea: Erpodellidae)" Experimental Parasitology , v.219 , 2020 https://doi.org/10.1016/j.exppara.2020.108002 Citation Details
Hobart, Brendan K. and Moss, Wynne E. and McDevittGalles, Travis and Stewart Merrill, Tara E. and Johnson, Pieter T. J. "It's a wormeatworm world: Consumption of parasite freeliving stages protects hosts and benefits predators" Journal of Animal Ecology , v.91 , 2021 https://doi.org/10.1111/1365-2656.13591 Citation Details
Johnson, Pieter and Calhoun, Dana M. and Moss, Wynne E. and McDevittGalles, Travis and Riepe, Tawni B. and Hallas, Joshua M. and Parchman, Thomas L. and Feldman, Chris R. and Achatz, Tyler J. and Tkach, Vasyl V. and Cropanzano, Josh and Bowerman, Jay and "The cost of travel: How dispersal ability limits local adaptation in hostparasite interactions" Journal of Evolutionary Biology , v.34 , 2020 https://doi.org/10.1111/jeb.13754 Citation Details
Johnson, Pieter T. and Calhoun, Dana M. and Riepe, Tawni and McDevitt-Galles, Travis and Koprivnikar, Janet "Community disassembly and disease: realistic?but not randomized?biodiversity losses enhance parasite transmission" Proceedings of the Royal Society B: Biological Sciences , v.286 , 2019 10.1098/rspb.2019.0260 Citation Details
Johnson, Pieter T. and Stewart Merrill, Tara E. and Dean, Andrew D. and Fenton, Andy "Diverging effects of host density and richness across biological scales drive diversity-disease outcomes" Nature Communications , v.15 , 2024 https://doi.org/10.1038/s41467-024-46091-4 Citation Details
Johnson, Pieter T. J. and Stewart Merrill, Tara and Calhoun, Dana M. and McDevittGalles, Travis and Hobart, Brendan "Into the danger zone: How the withinhost distribution of parasites controls virulence" Ecology Letters , v.27 , 2023 https://doi.org/10.1111/ele.14352 Citation Details
Koprivnikar, J. and Thieltges, D.W. and Johnson, P.T.J. "Consumption of trematode parasite infectious stages: from conceptual synthesis to future research agenda" Journal of Helminthology , v.97 , 2023 https://doi.org/10.1017/S0022149X23000111 Citation Details
Locke, Sean A. and Drago, Fabiana B. and López-Hernández, Danimar and Chibwana, Fred D. and Núñez, Verónica and Van Dam, Alex and Achinelly, María Fernanda and Johnson, Pieter T.J. and de Assis, Jordana Costa and de Melo, Alan Lane and Pinto, Hudson Alves "Intercontinental distributions, phylogenetic position and life cycles of species of Apharyngostrigea (Digenea, Diplostomoidea) illuminated with morphological, experimental, molecular and genomic data" International Journal for Parasitology , 2021 https://doi.org/10.1016/j.ijpara.2020.12.006 Citation Details
Martin, Kelly R. and Johnson, Pieter T. and Bowerman, Jay and Li, Jingchun "Biogeography of the freshwater gastropod, Planorbella trivolvis, in the western United States" PLOS ONE , v.15 , 2020 https://doi.org/10.1371/journal.pone.0235989 Citation Details
(Showing: 1 - 10 of 28)

PROJECT OUTCOMES REPORT

Disclaimer

This Project Outcomes Report for the General Public is displayed verbatim as submitted by the Principal Investigator (PI) for this award. Any opinions, findings, and conclusions or recommendations expressed in this Report are those of the PI and do not necessarily reflect the views of the National Science Foundation; NSF has not approved or endorsed its content.

With rising interest in understanding the links between diversity and infections, however, a polarizing debate has emerged over whether biodiversity generally decreases pathogen transmission (via the ‘dilution effect’), generally increases transmission (‘amplification effect’), or whether responses are idiosyncratic and highly variable among systems – issues that are especially contentious when it comes to management policies. Because evidence exists to support all of the above positions, a more productive approach may be to delineate under what host, parasite, and environmental conditions changes in diversity amplify or dilute disease risk. For most systems, however, we lack the essential combination of (1) empirical data from replicated communities, (2) parameterized transmission models, and (3) ecologically relevant experiments necessary to address these questions, particularly across a range of host and parasite taxa.

To address these missing links, we developed a predictive framework built on mechanistic approach to identify the conditions under which biodiversity affects the capacity of pathogens to spread or cause illness. Our research thus far has already significantly impacted the field of disease ecology generally and the study of the biodiversity-disease relationship more specifically. In the main, our finding has helped to address sources of confusion surrounding the diversity-disease relationship and specifically, understanding how changes in host community composition influence parasite transmission. We showed, for instance, that community level changes in infection levels owed to shifts in host species composition, rather than richness per se. However, when composition patterns mirrored empirical observations along a natural assembly gradient, each added host species reduced infection success by 12–55%. These findings highlight the potential for combining information on host traits and assembly patterns to forecast diversity-mediated changes in multi-host disease systems. We also examined how parasites themselves – through their choices in infecting specific host species within a community – alter the overall pattern of transmission in complex assemblages, particularly with trematodes which support complex communities and have multiple hosts. Using detailed experiments that tested parasite choice for alternative host species, both individually and through varying ‘choice sets,’ we showed that trematode cercariae demonstrated consistent and predictable preference patterns for specific host species; however, preferred hosts were not the most susceptible to infection, which is important for understanding whether forecasted shifts in diversity will alter overall infection success in multi-host communities.

Lastly, our work also made progress on the development of empirical and theoretical approaches for understanding diversity-disease relationships. We have built statistical models that are helping to assess the relative influence of proposed mechanisms underlying the influence of biodiversity losses on pathogen transmission, including shifts in host abundance, species composition, and predation. These findings emphasize the core importance of understanding the empirical relationship between species richness and species composition: thus, whether diversity leads to reduced parasite transmission depends critically on the degree to which the most competent hosts predominate in low-richness communities, which is a strongly consistent pattern in this system. For the four most closely studied trematode parasites, we found that host diversity leads to reductions in transmission both at the individual host scale (infection risk per host) and at the community scale (total parasite infection success among all co-occurring hosts). Yet the magnitude of these effects differed broadly. Empirical data from field surveys and laboratory experiments have contributed to four manuscripts related to (1) deterministic patterns in ecological community assembly, (2) variation in competence across host-parasite-dosage combinations throughout communities, (3) a review of the epidemiological concept of competence and identification of core knowledge gaps, and (4) empirical analysis of field data to assess how richness, density, and predators affect transmission of different trematodes and at two biological scales (host level vs. community level).

 

Broader impacts:

This research capitalized on the public’s interest in amphibians generally – and in amphibian deformities specifically – to foster educational outreach and conservation awareness. PI Johnson and supported science personnel (Dana Calhoun) worked closely with students across a range of educational levels and backgrounds to foster research aptitude, encourage science career opportunities, and promote recruitment by under-represented groups. Partnering with programs such as the Colorado Initiative, the Science Discovery Center, Undergraduate Research Opportunities Program (UROP), and the Biological Science Initiative (BSI), this grant provided experiential research opportunities for 24 undergraduates and 20 technicians. In addition, we supported a RAHSS student, 4 REU students, three graduate students, and a postdoctoral researcher. To reach the public and disseminate research finding nearly 13 talks were given across multiple venues (e.g. Zoological Society of London, Wildlife Disease Association Meeting, California-Nevada Amphibian Population Task Force and, American Society of Parasitologist, Ecology and Evolution of Infectious Disease). In addition of the 27 peer-reviewed publications produced by this project, 12 included undergraduate or graduate student co-authors and 8 were lead-authored by a student.

 


Last Modified: 04/15/2025
Modified by: Pieter T Johnson

Please report errors in award information by writing to: awardsearch@nsf.gov.

Print this page

Back to Top of page