Parasite load and site-specific parasite pressure as determinants of immune indices in two sympatric rodent species

Tim R. Hofmeester, Esther J. Bügel, Bob Hendrikx, Miriam Maas, Frits F.J. Franssen, Hein Sprong, Kevin D. Matson*

*Corresponding author for this work

Research output: Contribution to journalArticleAcademicpeer-review

Abstract

Wildlife is exposed to parasites from the environment. This parasite pressure, which differs among areas, likely shapes the immunological strategies of animals. Individuals differ in the number of parasites they encounter and host, and this parasite load also influences the immune system. The relative impact of parasite pressure vs. parasite load on different host species, particularly those implicated as important reservoirs of zoonotic pathogens, is poorly understood. We captured bank voles (Myodes glareolus) and wood mice (Apodemus sylvaticus) at four sites in the Netherlands. We sampled sub-adult males to quantify their immune function, infestation load for ecto-and gastrointestinal parasites, and infection status for vector-borne microparasites. We then used regression trees to test if variation in immune indices could be explained by among-site differences (parasite pressure), among-individual differences in infestation intensity and infection status (parasite load), or other intrinsic factors. Regression trees revealed splits among sites for haptoglobin, hemagglutination, and body-mass corrected spleen size. We also found splits based on infection/infestation for haptoglobin, hemolysis, and neutrophil to lymphocyte ratio. Furthermore, we found a split between species for hemolysis and splits based on body mass for haptoglobin, hemagglutination, hematocrit, and body-mass corrected spleen size. Our results suggest that both parasite pressure and parasite load influence the immune system of wild rodents. Additional studies linking disease ecology and ecological immunology are needed to understand better the complexities of host–parasite interactions and how these interactions shape zoonotic disease risk.

Original languageEnglish
Article number1015
JournalAnimals
Volume9
Issue number12
DOIs
Publication statusPublished - 1 Dec 2019

Fingerprint

Parasite Load
Sympatry
parasite load
Rodentia
Parasites
rodents
Pressure
parasites
Haptoglobins
haptoglobins
Arvicolinae
Zoonoses
Hemagglutination
Clethrionomys glareolus
Hemolysis
hemolysis
hemagglutination
Immune System
Spleen
immune system

Keywords

  • Ecological immunology
  • Haptoglobin
  • Immune strategy
  • Natural antibodies
  • Neutrophil to lymphocyte ratio
  • Parasitology
  • Rodents
  • Vector-borne pathogens
  • Zoonosis

Cite this

Hofmeester, T. R., Bügel, E. J., Hendrikx, B., Maas, M., Franssen, F. F. J., Sprong, H., & Matson, K. D. (2019). Parasite load and site-specific parasite pressure as determinants of immune indices in two sympatric rodent species. Animals, 9(12), [1015]. https://doi.org/10.3390/ani9121015
Hofmeester, Tim R. ; Bügel, Esther J. ; Hendrikx, Bob ; Maas, Miriam ; Franssen, Frits F.J. ; Sprong, Hein ; Matson, Kevin D. / Parasite load and site-specific parasite pressure as determinants of immune indices in two sympatric rodent species. In: Animals. 2019 ; Vol. 9, No. 12.
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abstract = "Wildlife is exposed to parasites from the environment. This parasite pressure, which differs among areas, likely shapes the immunological strategies of animals. Individuals differ in the number of parasites they encounter and host, and this parasite load also influences the immune system. The relative impact of parasite pressure vs. parasite load on different host species, particularly those implicated as important reservoirs of zoonotic pathogens, is poorly understood. We captured bank voles (Myodes glareolus) and wood mice (Apodemus sylvaticus) at four sites in the Netherlands. We sampled sub-adult males to quantify their immune function, infestation load for ecto-and gastrointestinal parasites, and infection status for vector-borne microparasites. We then used regression trees to test if variation in immune indices could be explained by among-site differences (parasite pressure), among-individual differences in infestation intensity and infection status (parasite load), or other intrinsic factors. Regression trees revealed splits among sites for haptoglobin, hemagglutination, and body-mass corrected spleen size. We also found splits based on infection/infestation for haptoglobin, hemolysis, and neutrophil to lymphocyte ratio. Furthermore, we found a split between species for hemolysis and splits based on body mass for haptoglobin, hemagglutination, hematocrit, and body-mass corrected spleen size. Our results suggest that both parasite pressure and parasite load influence the immune system of wild rodents. Additional studies linking disease ecology and ecological immunology are needed to understand better the complexities of host–parasite interactions and how these interactions shape zoonotic disease risk.",
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Parasite load and site-specific parasite pressure as determinants of immune indices in two sympatric rodent species. / Hofmeester, Tim R.; Bügel, Esther J.; Hendrikx, Bob; Maas, Miriam; Franssen, Frits F.J.; Sprong, Hein; Matson, Kevin D.

In: Animals, Vol. 9, No. 12, 1015, 01.12.2019.

Research output: Contribution to journalArticleAcademicpeer-review

TY - JOUR

T1 - Parasite load and site-specific parasite pressure as determinants of immune indices in two sympatric rodent species

AU - Hofmeester, Tim R.

AU - Bügel, Esther J.

AU - Hendrikx, Bob

AU - Maas, Miriam

AU - Franssen, Frits F.J.

AU - Sprong, Hein

AU - Matson, Kevin D.

PY - 2019/12/1

Y1 - 2019/12/1

N2 - Wildlife is exposed to parasites from the environment. This parasite pressure, which differs among areas, likely shapes the immunological strategies of animals. Individuals differ in the number of parasites they encounter and host, and this parasite load also influences the immune system. The relative impact of parasite pressure vs. parasite load on different host species, particularly those implicated as important reservoirs of zoonotic pathogens, is poorly understood. We captured bank voles (Myodes glareolus) and wood mice (Apodemus sylvaticus) at four sites in the Netherlands. We sampled sub-adult males to quantify their immune function, infestation load for ecto-and gastrointestinal parasites, and infection status for vector-borne microparasites. We then used regression trees to test if variation in immune indices could be explained by among-site differences (parasite pressure), among-individual differences in infestation intensity and infection status (parasite load), or other intrinsic factors. Regression trees revealed splits among sites for haptoglobin, hemagglutination, and body-mass corrected spleen size. We also found splits based on infection/infestation for haptoglobin, hemolysis, and neutrophil to lymphocyte ratio. Furthermore, we found a split between species for hemolysis and splits based on body mass for haptoglobin, hemagglutination, hematocrit, and body-mass corrected spleen size. Our results suggest that both parasite pressure and parasite load influence the immune system of wild rodents. Additional studies linking disease ecology and ecological immunology are needed to understand better the complexities of host–parasite interactions and how these interactions shape zoonotic disease risk.

AB - Wildlife is exposed to parasites from the environment. This parasite pressure, which differs among areas, likely shapes the immunological strategies of animals. Individuals differ in the number of parasites they encounter and host, and this parasite load also influences the immune system. The relative impact of parasite pressure vs. parasite load on different host species, particularly those implicated as important reservoirs of zoonotic pathogens, is poorly understood. We captured bank voles (Myodes glareolus) and wood mice (Apodemus sylvaticus) at four sites in the Netherlands. We sampled sub-adult males to quantify their immune function, infestation load for ecto-and gastrointestinal parasites, and infection status for vector-borne microparasites. We then used regression trees to test if variation in immune indices could be explained by among-site differences (parasite pressure), among-individual differences in infestation intensity and infection status (parasite load), or other intrinsic factors. Regression trees revealed splits among sites for haptoglobin, hemagglutination, and body-mass corrected spleen size. We also found splits based on infection/infestation for haptoglobin, hemolysis, and neutrophil to lymphocyte ratio. Furthermore, we found a split between species for hemolysis and splits based on body mass for haptoglobin, hemagglutination, hematocrit, and body-mass corrected spleen size. Our results suggest that both parasite pressure and parasite load influence the immune system of wild rodents. Additional studies linking disease ecology and ecological immunology are needed to understand better the complexities of host–parasite interactions and how these interactions shape zoonotic disease risk.

KW - Ecological immunology

KW - Haptoglobin

KW - Immune strategy

KW - Natural antibodies

KW - Neutrophil to lymphocyte ratio

KW - Parasitology

KW - Rodents

KW - Vector-borne pathogens

KW - Zoonosis

U2 - 10.3390/ani9121015

DO - 10.3390/ani9121015

M3 - Article

VL - 9

JO - Animals

JF - Animals

SN - 2076-2615

IS - 12

M1 - 1015

ER -

Hofmeester TR, Bügel EJ, Hendrikx B, Maas M, Franssen FFJ, Sprong H et al. Parasite load and site-specific parasite pressure as determinants of immune indices in two sympatric rodent species. Animals. 2019 Dec 1;9(12). 1015. https://doi.org/10.3390/ani9121015