Skip to main content

Advertisement

SpringerLink
Log in

Zoonotic Disease Risk and Life-History Traits: Are Reservoirs Fast Life Species?

  • Original Contribution
  • Published:
EcoHealth Aims and scope Submit manuscript

Abstract

The relationship between humans, wildlife and disease transmission can be complex and context-dependent, and disease dynamics may be determined by idiosyncratic species. Therefore, an outstanding question is how general is the finding that species with faster life histories are more probable hosts of zoonoses. Ecological knowledge on species, jointly with public health data, can provide relevant information on species that should be targeted for epidemiological surveillance or management. We investigated whether mammal species traits can be good indicators of zoonotic reservoir status in an intensified agricultural region of Argentina. We find support for a relationship between reservoir status and the pace of life syndrome, confirming that fast life histories can be a factor of zoonotic risk. Nonetheless, we observed that for certain zoonosis, reservoirs may display a slow pace of life, suggesting that idiosyncratic interactions can occur. We conclude that applying knowledge from the life history-disease relationship can contribute significantly to disease risk assessment. Such an approach may be especially valuable in the current context of environmental change and agricultural intensification.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5

Similar content being viewed by others

Data Availability

The datasets generated and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  • Albery GF, Becker DJ (2020) Fast-lived Hosts and Zoonotic Risk. Trends in Parasitology 37(2):117–129

    Article  PubMed  CAS  Google Scholar 

  • Allen T, Murray KA, Zambrana-Torrelio C, Morse SS, Rondinini C, Di Marco M, Breit N, Olival KJ, Daszak P (2017) Global hotspots and correlates of emerging zoonotic diseases. Nature Communications 8:1–10

    Article  CAS  Google Scholar 

  • Barquez RM, Diaz MM, Ojeda RA (2006) Mamiferos de Argentina. Sistemática y Distribución Editorial SAREM, Mendoza, Argentina 375

  • Becker DJ, Streicker DG, Altizer S (2018) Using host species traits to understand the consequences of resource provisioning for host-parasite interactions. Journal of Animal Ecology 87:511–525

    Article  PubMed  Google Scholar 

  • Belay ED, Kile JC, Hall AJ, Barton-Behravesh C, Parsons MB, Salyer S, Walke H (2017) Zoonotic disease programs for enhancing global health security. Emerging Infectious Diseases 23:S65

    Article  PubMed Central  Google Scholar 

  • Bielby J, Mace GM, Bininda-Emonds OR, Cardillo M, Gittleman JL, Jones KE, Orme CDL, Purvis A (2007) The fast-slow continuum in mammalian life history: an empirical reevaluation. The American Naturalist 169:748–757

    Article  PubMed  CAS  Google Scholar 

  • Bilenca D, Codesido M, González Fisher C, Perez Carusi L (2009) Impactos de la actividad agropecuaria sobre la biodiversidad en la ecorregión pampeana: impactos de la expansión agricola y de la intensificación de la agricultura y la ganaderia de campo, con algunas recomendaciones de manejo para su mitigación. Ediciones INTA, Buenos Aires

  • Bó MS, Isacch JP, Malizia AI, Martinez MM (2002) Lista comentada de los mamiferos de la Reserva de Biósfera Mar Chiquita, provincia de Buenos Aires, Argentina. Mastozoologia Neotropical 9:5–11

    Google Scholar 

  • Broglia A, Kapel C (2011) Changing dietary habits in a changing world: emerging drivers for the transmission of foodborne parasitic zoonoses. Veterinary Parasitology 182:2–13

    Article  PubMed  CAS  Google Scholar 

  • Dallas TA, Han BA, Nunn CL, Park AW, Stephens PR, Drake JM (2019) Host traits associated with species roles in parasite sharing networks. Oikos 128:23–32

    Article  Google Scholar 

  • Daszak P, Cunningham A, Hyatt A (2000) Emerging infectious diseases of wildlife-threats to biodiversity and human health. Science 287:443–449

    Article  PubMed  CAS  Google Scholar 

  • Enria DA, Pinheiro F (2000) Rodent-borne emerging viral zoonosis: hemorrhagic fevers and hantavirus infections in South America. Infectious Disease Clinics of North America 14:167–184

    Article  PubMed  CAS  Google Scholar 

  • Ernest SM (2003) Life history characteristics of placental nonvolant mammals: ecological archives E084–093. Ecology 84:3402–3402

    Article  Google Scholar 

  • Estrada-Peña A, Ostfeld RS, Peterson AT, Poulin R, de la Fuente J (2014) Effects of environmental change on zoonotic disease risk: an ecological primer. Trends in Parasitology 30:205–214

    Article  PubMed  Google Scholar 

  • Gaillard J-M, Lemaitre J-F, Berger V, Bonenfant C, Devillard S, Douhard M, Gamelon M, Plard F, Lebreton J (2016) Life histories, axes of variation in. In: Kliman RM (ed) Encyclopedia of evolutionary biology, vol 2. Oxford: Academic Press, pp 312–323

    Chapter  Google Scholar 

  • Gaillard J-M, Yoccoz NG, Lebreton J-D, Bonenfant C, Devillard S, Loison A, Pontier D, Allaine D (2005) Generation time: a reliable metric to measure life-history variation among mammalian populations. The American Naturalist 166:119–123

    Article  PubMed  Google Scholar 

  • Gibb R, Redding D, Qing Chin K, Donnelly C, Blackburn T, Newbold T, Jones K (2020) Zoonotic host diversity increases in human-dominated ecosystems. Nature 584(7821):398–402

    Article  PubMed  CAS  Google Scholar 

  • Gomez MD, Coda J, Simone I, Martinez J, Bonatto F, Steinmann AR, Priotto J (2015) Agricultural land-use intensity and its effects on small mammals in the central region of Argentina. Mammal Research 60:415–423

    Article  Google Scholar 

  • González Fischer CM, Cavia R, Picasso P, Bilenca D (2017) Regional and local determinants of rodent assemblages in agroecosystems of the Argentine Pampas. Journal of Mammalogy 98:1760–1767

    Article  Google Scholar 

  • Guo F, Bonebrake TC, Gibson L (2019) Land-use change alters host and vector communities and may elevate disease risk. Ecohealth 16:647–658

    Article  PubMed  Google Scholar 

  • Han BA, O’Regan SM, Paul Schmidt J, Drake JM (2020) Integrating data mining and transmission theory in the ecology of infectious diseases. Ecology Letters 23(8):1178–1188

    Article  PubMed  PubMed Central  Google Scholar 

  • Han BA, Schmidt JP, Bowden SE, Drake JM (2015) Rodent reservoirs of future zoonotic diseases. Proceedings of the National Academy of Sciences 112:7039–7044

    Article  CAS  Google Scholar 

  • Huang ZY, de Boer WF, van Langevelde F, Olson V, Blackburn TM, Prins HH (2013) Species’ life-history traits explain interspecific variation in reservoir competence: a possible mechanism underlying the dilution effect. PLoS One 8:e54341

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Johnson PT, Ostfeld RS, Keesing F (2015) Frontiers in research on biodiversity and disease. Ecology Letters 18:1119–1133

    Article  PubMed  PubMed Central  Google Scholar 

  • Johnson PTJ, Rohr JR, Hoverman JT, Kellermanns E, Bowerman J, Lunde KB (2012) Living fast and dying of infection: host life history drives interspecific variation in infection and disease risk. Ecology Letters 15:235–242

    Article  PubMed  Google Scholar 

  • Jones BA, Grace D, Kock R, Alonso S, Rushton J, Said MY, McKeever D, Mutua F, Young J, McDermott J, Pfeiffer DU (2013) Zoonosis emergence linked to agricultural intensification and environmental change. Proceedings of the National Academy of Sciences 110:8399–8404

    Article  Google Scholar 

  • Jones KE, Bielby J, Cardillo M, Fritz SA, O’Dell J, Orme CDL, Safi K, Sechrest W, Boakes EH, Carbone C, Connolly C, Cutts MJ, Foster JK, Grenyer R, Habib M, Plaster CA, Price SA, Rigby EA, Rist J, Teacher A, Bininda-Emonds ORP, Gittleman JL, Mace GM, Purvis A, Michener W (2009) PanTHERIA: a species-level database of life history, ecology, and geography of extant and recently extinct mammals: Ecological Archives E090–184. Ecology 90:2648–2648

    Article  Google Scholar 

  • Karesh WB, Dobson A, Lloyd-Smith JO, Lubroth J, Dixon MA, Bennett M, Aldrich S, Harrington T, Formenty P, Loh EH, Machalaba CC, Thomas MJ, Heymann DL (2012) Ecology of zoonoses: natural and unnatural histories. Lancet 380:1936–1945. https://doi.org/10.1016/S0140-6736(12)61678-X

    Article  PubMed  PubMed Central  Google Scholar 

  • Keesing F, Belden LK, Daszak P, Dobson A, Harvell CD, Holt RD, Hudson P, Jolles A, Jones KE, Mitchell CE, Myers SS, Bogich T, Ostfeld RS (2010) Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature 468:647–652

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Legendre P, Legendre L (1998) Numerical ecology: second, English. Elsevier

    Google Scholar 

  • Massa C, Teta P, Cueto GR (2014) Effects of regional context and landscape composition on diversity and composition of small rodent assemblages in Argentinian temperate grasslands and wetlands. Mammalia 78:371–382

    Article  Google Scholar 

  • Medan D, Torretta JP, Hodara K, Elba B, Montaldo NH (2011) Effects of agriculture expansion and intensification on the vertebrate and invertebrate diversity in the Pampas of Argentina. Biodiversity and Conservation 20:3077–3100

    Article  Google Scholar 

  • Mendoza H, Rubio AV, García-Peña GE, Suzán G, Simonetti JA (2020) Does land-use change increase the abundance of zoonotic reservoirs? Rodents say yes. European Journal of Wildlife Research 66(1):1–5

    Article  Google Scholar 

  • Modernel P, Rossing WA, Corbeels M, Dogliotti S, Picasso V, Tittonell P (2016) Land use change and ecosystem service provision in Pampas and Campos grasslands of southern South America. Environmental Research Letters 11:113002

    Article  Google Scholar 

  • Nanni AS, Rodriguez MP, Rodriguez D, Regueiro MN, Periago ME, Aguiar S, Ballari S, Blundo C, Derlindati E, Di Blanco Y, Eljall A, Grau HR, Herrera LP, Huertas Herrera A, Izquierdo AE, Lescano JN, Macchi L, Mazzini F, Milkovic M, Quintana RD, Quiroga VA, Reniso D, Beade Santos M, Schaaf AA, Gasparri NI (2020) Presiones sobre la conservación asociadas al uso de la tierra en las ecorregiones terrestres de la Argentina. Ecologia Austral 30:304–320

    Article  Google Scholar 

  • Narrod C, Zinsstag J, Tiongco M (2012) A one health framework for estimating the economic costs of zoonotic diseases on society. Ecohealth 9:150–162

    Article  PubMed  PubMed Central  Google Scholar 

  • O’Regan SM, Drake JM (2013) Theory of early warning signals of disease emergenceand leading indicators of elimination. Theoretical Ecology 6:333–357

    Article  PubMed  PubMed Central  Google Scholar 

  • Olival KJ, Hosseini PR, Zambrana-Torrelio C, Ross N, Bogich TL, Daszak P (2017) Host and viral traits predict zoonotic spillover from mammals. Nature 546:646–650

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ostfeld RS, Levi T, Jolles AE, Martin LB, Hosseini PR, Keesing F (2014) Life history and demographic drivers of reservoir competence for three tick-borne zoonotic pathogens. PLoS One 9:e107387

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pacifici M, Santini L, Di Marco M, Baisero D, Francucci L, Marasini GG, Visconti P, Rondinini C (2013) Generation Length for Mammals. Nature Conservation 5:89

    Article  Google Scholar 

  • Pengue WA (2005) Transgenic crops in Argentina: the ecological and social debt. Bulletin of Science, Technology & Society 25:314–322

    Article  Google Scholar 

  • Piacenza MF, Calderón GE, Enria D, Provensal MC, Polop JJ (2018) Diferencia espacial de la incidencia de fiebre hemorrágica argentina y la composición y abundancia de roedores en el ensamble. Revista Chilena De Infectologia 35:386–394

    Article  PubMed  Google Scholar 

  • Plourde BT, Burgess TL, Eskew EA, Roth TM, Stephenson N, Foley JE (2017) Are disease reservoirs special? Taxonomic and life history characteristics. PLoS One 12:e0180716

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Previtali MA, Ostfeld RS, Keesing F, Jolles AE, Hanselmann R, Martin LB (2012) Relationship between pace of life and immune responses in wild rodents. Oikos 121:1483–1492

    Article  Google Scholar 

  • Prist PR, Metzger JP (2017) Landscape, climate and hantavirus cardiopulmonary syndrome outbreaks. Ecohealth 14:614–629

    Article  PubMed  Google Scholar 

  • Raffard A, Lecerf A, Cote J, Buoro M, Lassus R, Cucherousset J (2017) The functional syndrome: linking individual trait variability to ecosystem functioning. Proceedings of the Royal Society b: Biological Sciences 284:20171893

    Article  PubMed  PubMed Central  Google Scholar 

  • Ricklefs RE, Wikelski M (2002) The physiology/life-history nexus. Trends in Ecology & Evolution 17:462–468

    Article  Google Scholar 

  • Rohr JR, Barrett CB, Civitello DJ, Craft ME, Delius B, DeLeo GA, Hudson PJ, Jouanard N, Nguyen KH, Ostfeld RS, Remais JV, Riveau G, Sokolow SH, Tilman D (2019) Emerging human infectious diseases and the links to global food production. Nature Sustainability 2:445–456

    Article  PubMed  PubMed Central  Google Scholar 

  • Salkeld DJ, Padgett KA, Jones JH (2013) A meta-analysis suggesting that the relationship between biodiversity and risk of zoonotic pathogen transmission is idiosyncratic. Ecology Letters 16:679–686. https://doi.org/10.1111/ele.12101

    Article  PubMed  PubMed Central  Google Scholar 

  • Silk MJ, Hodgson DJ (2021) Life history and population regulation shape demographic competence and influence the maintenance of endemic disease. Nature Ecology & Evolution 5(1):82–91

    Article  Google Scholar 

  • Urcola HA, De Sartre XA, Veiga I Jr, Elverdin J, Albaladejo C (2015) Land tenancy, soybean, actors and transformations in the pampas: A district balance. Journal of Rural Studies 39:32–40

    Article  Google Scholar 

  • Valenzuela-Sánchez A, Wilber MQ, Canessa S, Bacigalupe LD, Muths E, Schmidt BR, Cunningham AA, Ozgul A, Johnson PT, Cayuela H (2021) Why disease ecology needs life-history theory: a host perspective. Ecology Letters 24:876–890

    Article  PubMed  Google Scholar 

  • Velasco MA, Lutz MA, Berkunsky I, Kacoliris FP, López Santoro MS (2013) Mammals of protected area“ La Poligonal” and neighborhood areas in Tandilia hills, Buenos Aires, Argentina. Check List 9:1510–1513

    Google Scholar 

  • Wu J, Yonezawa T, Kishino H (2021) Evolution of Reproductive Life History in Mammals and the Associated Change of Functional Constraints. Genes (basel) 12:740

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank the editor and two anonymous reviewers for their constructive comments, which helped us to improve the manuscript. We want to thank Dr. Federico Costa for his advice on Leptospirosis and its reservoirs. We thank Dr. Marcos Grigioni for his comments on early version of the manuscript. This work was supported by the Consejo Nacional de Investigaciones Cientificas y Tecnicas of Argentina (CONICET) and a Postdoctoral fellowship (RESOL-2020-134-APN-DIR#CONICET) to Candelaria Estavillo. We would like to thank the Grupo de Estudios de Agroecosistemas y Paisajes Rurales (GEAP) for the fruitful discussions that helped to improve this manuscript.

Author information

Authors and Affiliations

  1. Grupo de Estudio de Agroecosistemas y Paisajes Rurales, Facultad de Ciencias Agrarias, Universidad Nacional de Mar del Plata, CONICET, EEI INTA Balcarce, Ruta 226 Km 73.5, Balcarce, Prov. de Buenos Aires, Argentina

    Candelaria Estavillo, Federico Weyland & Lorena Herrera

Authors
  1. Candelaria Estavillo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Federico Weyland
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lorena Herrera
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Candelaria Estavillo.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Human and Animal Rights

This article does not contain any studies with human participants or animals performed by any of the authors.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file 1 (DOCX 118 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Estavillo, C., Weyland, F. & Herrera, L. Zoonotic Disease Risk and Life-History Traits: Are Reservoirs Fast Life Species?. EcoHealth 19, 390–401 (2022). https://doi.org/10.1007/s10393-022-01608-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10393-022-01608-5

Keywords

Search

Navigation