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Variation in leukocyte indices and immunoglobulin levels according to host density, sex, flea burden and tularemia prevalence in the common vole Microtus arvalis

  • François Mougeot , Manuel B. Morales EMAIL logo , María José Pérez Álvarez , Miguel Muñoz López , Ruth Rodríguez-Pastor and Juan José Luque-Larena
Published/Copyright: January 3, 2024
Mammalia
From the journal Mammalia Volume 88 Issue 2

Abstract

Rodent populations often undergo large, regular fluctuations. We studied immunological condition and physiological stress in the common vole and how it varied with environmental factors linked with population fluctuations, namely flea and Francisella tularensis (the bacterium causing tularemia) prevalence. We used two leukocyte indices, neutrophil-to-lymphocyte ratio (N:L) and proportion of eosinophils, as physiological long-term stress indicators, and measured levels of immunoglobulins (Ig) as a generic index of immunological condition. Leukocyte indices showed a hump-shaped relationship with Ig levels, consistent with an interdependence between physiological stress and immunological condition. N:L was negatively associated with vole density only in males. Eosinophil proportion was explained by the interaction between flea burden and tularemia prevalence, with highest levels in flea-infested voles also infected with tularemia. Ig levels did not vary with sex or flea prevalence but increased in tularemia-infected voles. When Ig levels were included as covariates in our models, the associations between leukocyte indices and environmental factors remained significant. Results suggest sex-specific associations between physiological stress and population density, and an influence of tularemia infection depending on ectoparasite load. We recommend using immunological parameters complementarily to leukocyte indices when studying physiological stress and infection dynamics in wild populations.

Keywords: eosinophils; ectoparasite; flea; neutrophil-to-lymphocyte ratio; population density; tularemia
Corresponding author: Manuel B. Morales, Departamento de Ecología and Research Centre in Biodiversity and Global Change, Universidad Autónoma de Madrid (Edificio de Biología), C/Darwin 2, 28049 Madrid, Spain, E-mail:

Funding source: MINECO of Spain

Award Identifier / Grant number: (projects ECOTULA CGL2015-66962-C2-1-R, BOOMRAT PID2019-109327RB-I00 and RATALERT PID2022-136850NB-I00)

Funding source: The Comunidad de Madrid (REMEDINAL 3)

Acknowledgments

We thank JL Guzmán, J Caro, J Romairone, MF Flechoso and R Escudero for their help with fieldwork, ectoparasite identification and tularemia detection. We also thank AI López-Archilla for her assistance with inverted microscopy.

  1. Research ethics: All the necessary ethic and capture permits for these procedures were provided by the Government of Castilla y León (Consejería de Fomento y Medio Ambiente, Junta de Castilla y León). The protocol for vole euthanasia was approved by the Universidad de Valladolid ethics committee (CEEBA, authorization code: 4801646). FM, RRP and JJLL held animal experimentation permits of level C for Spain. Common voles’ carcasses are currently kept at the University of Valladolid (Escuela Técnica Superior de Ingenieros Agrónomos, campus of Palencia, Spain) under the custody of Prof. Juan José Luque Larena.

  2. Author contributions: FM, JJLL, MJPA and MBM conceptualized the study, RRP, FM and JJLL captured and processed the voles at the laboratory, MML examined all blood smears and run the Ig electrophoresis experiments under the supervision of MJPA. RRP was responsible for the molecular Tularemia infection detection. FM analyzed the data. FM, MBM and MJPA wrote the ms and all authors reviewed and commented on successive versions.

  3. Competing interests: The authors state that there is no conflict of interest regarding this manuscript.

  4. Research funding: Funding was provided by the MINECO of Spain (projects ECOTULA CGL2015-66962-C2-1-R, BOOMRAT PID2019-109327RB-I00 and RATALERT PID2022-136850NB-I00) and the Comunidad de Madrid (REMEDINAL 3).

  5. Data availability: The raw data can be obtained on request from the corresponding author.

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Supplementary Material

This article contains supplementary material (https://doi.org/10.1515/mammalia-2023-0090).

Received: 2023-07-23
Accepted: 2023-11-24
Published Online: 2024-01-03
Published in Print: 2024-03-25

© 2023 Walter de Gruyter GmbH, Berlin/Boston

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https://doi.org/10.1515/mammalia-2023-0090
Keywords for this article
eosinophils; ectoparasite; flea; neutrophil-to-lymphocyte ratio; population density; tularemia

Articles in the same Issue

  1. Frontmatter
  2. Ecology
  3. Insights into surveying pangolins using ground and arboreal camera traps
  4. Reproductive aspects of female Andean bears (Tremarctos ornatus) in the Chingaza massif, eastern range of the Colombian Andes
  5. Using photo by-catch data to reliably estimate spotted hyaena densities over time
  6. Review of ocular alterations in bats in America and notes on a new case for Saccopteryx bilineata (Chiroptera: Emballonuridae)
  7. New dietary records for the rare Thomas’s Flying Squirrel (Aeromys thomasi, Sciuridae: Pteromyini) from Sabah, Malaysian Borneo
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  12. Evolutionary Biology
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