Loading…

Effects of manipulated food availability and seasonality on innate immune function in a passerine

The innate immune system is essential for survival, yet many immune traits are highly variable between and within individuals. In recent years, attention has shifted to the role of environmental factors in modulating this variation. A key environmental factor is food availability, which plays a majo...

Full description

Saved in:
Bibliographic Details
Published in:The Journal of animal ecology 2022-12, Vol.91 (12), p.2400-2411
Main Authors: Driessen, Merijn M. G., Versteegh, Maaike A., Gerritsma, Yoran H., Tieleman, B. Irene, Pen, Ido R., Verhulst, Simon
Format: Article
Language:English
Subjects:
Citations: Items that this one cites
Online Access:Get full text
Tags: Add Tag
No Tags, Be the first to tag this record!
cited_by
cites cdi_FETCH-LOGICAL-c4232-93b6704ac77f1be4cc9c21a2b6245be1d26915836859ee1c90fa7ad9aa5541073
container_end_page 2411
container_issue 12
container_start_page 2400
container_title The Journal of animal ecology
container_volume 91
creator Driessen, Merijn M. G.
Versteegh, Maaike A.
Gerritsma, Yoran H.
Tieleman, B. Irene
Pen, Ido R.
Verhulst, Simon
description The innate immune system is essential for survival, yet many immune traits are highly variable between and within individuals. In recent years, attention has shifted to the role of environmental factors in modulating this variation. A key environmental factor is food availability, which plays a major role in shaping life histories, and may affect resource allocation to immune function through its effect on nutritional state. We developed a technique to permanently increase foraging costs in seed‐eating birds, and leveraged this technique to study the effects of food availability on the innate immune system over a 3‐year period in 230 zebra finches housed in outdoor aviaries. The immune components we studied were haptoglobin, ovotransferrin, nitric oxide, natural antibodies through agglutination, complement‐mediated lysis, and killing capacity of Escherichia coli and Candida albicans, covering a broad spectrum of the innate immune system. We explored the effects of food availability in conjunction with other potentially important variables: season, age, sex and manipulated natal brood size. Increased foraging costs affected multiple components of the immune system, albeit in a variable way. Nitric oxide and agglutination levels were lower under harsh foraging conditions, while Escherichia coli killing capacity was increased. Agglutination levels also varied seasonally, but only at low foraging costs. C. albicans killing capacity was lower in winter, and even more so for animals in harsh foraging conditions that were raised in large broods. Effects of food availability on ovotransferrin were also seasonal, and only apparent in males. Haptoglobin levels were independent of foraging costs and season. Males had higher levels of immune function than females for three of the measured immune traits. Innate immune function was independent of age and manipulated natal brood size. Our finding that food availability affects innate immune function suggests that fitness effects of food availability may at least partially be mediated by effects on the immune system. However, food availability effects on innate immunity varied in direction between traits, illustrating the complexity of the immune system and precluding conclusions on the level of disease resistance. This paper explores the effects of an ecologically relevant manipulation of foraging effort on a broad array of six innate immune measures, while also looking at effects of development, season and sex.
doi_str_mv 10.1111/1365-2656.13822
format article
fullrecord <record><control><sourceid>proquest_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_10092825</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>2727642516</sourcerecordid><originalsourceid>FETCH-LOGICAL-c4232-93b6704ac77f1be4cc9c21a2b6245be1d26915836859ee1c90fa7ad9aa5541073</originalsourceid><addsrcrecordid>eNqFkU1v1DAQhi0EotuFMzdkiQuXtP6I7eSEqmopoAoucLYmzhhcJfYSJ6323-PdLSvgwlwsjx-_such5BVnF7zUJZdaVUIrfcFlI8QTsjp1npIVY4JXjWnZGTnP-Y4xZgSTz8mZ1EI3uhUrAhvv0c2ZJk9HiGG7DDBjT31KPYV7CAN0YQjzjkLsaUbIKcJhnyINMRaYhnFcIlK_RDeHQ5sC3ULOOIWIL8gzD0PGl4_rmnx7v_l6_aG6_XLz8frqtnK1kKJqZacNq8EZ43mHtXOtExxEp0WtOuS90C1XjdSNahG5a5kHA30LoFTNmZFr8u6Yu126EXuHcZ5gsNspjDDtbIJg_z6J4Yf9nu4tZ6wVjVAl4e1jwpR-LphnO4bscBggYlqyFUYYXQvFdUHf_IPepWUqk9lTdZlyI0utyeWRclPKeUJ_eg1ndu_P7m3ZvS178FduvP7zEyf-t7AC6CPwEAbc_S_Pfrr6vDkm_wKtAaXk</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2747208333</pqid></control><display><type>article</type><title>Effects of manipulated food availability and seasonality on innate immune function in a passerine</title><source>Wiley</source><creator>Driessen, Merijn M. G. ; Versteegh, Maaike A. ; Gerritsma, Yoran H. ; Tieleman, B. Irene ; Pen, Ido R. ; Verhulst, Simon</creator><creatorcontrib>Driessen, Merijn M. G. ; Versteegh, Maaike A. ; Gerritsma, Yoran H. ; Tieleman, B. Irene ; Pen, Ido R. ; Verhulst, Simon</creatorcontrib><description>The innate immune system is essential for survival, yet many immune traits are highly variable between and within individuals. In recent years, attention has shifted to the role of environmental factors in modulating this variation. A key environmental factor is food availability, which plays a major role in shaping life histories, and may affect resource allocation to immune function through its effect on nutritional state. We developed a technique to permanently increase foraging costs in seed‐eating birds, and leveraged this technique to study the effects of food availability on the innate immune system over a 3‐year period in 230 zebra finches housed in outdoor aviaries. The immune components we studied were haptoglobin, ovotransferrin, nitric oxide, natural antibodies through agglutination, complement‐mediated lysis, and killing capacity of Escherichia coli and Candida albicans, covering a broad spectrum of the innate immune system. We explored the effects of food availability in conjunction with other potentially important variables: season, age, sex and manipulated natal brood size. Increased foraging costs affected multiple components of the immune system, albeit in a variable way. Nitric oxide and agglutination levels were lower under harsh foraging conditions, while Escherichia coli killing capacity was increased. Agglutination levels also varied seasonally, but only at low foraging costs. C. albicans killing capacity was lower in winter, and even more so for animals in harsh foraging conditions that were raised in large broods. Effects of food availability on ovotransferrin were also seasonal, and only apparent in males. Haptoglobin levels were independent of foraging costs and season. Males had higher levels of immune function than females for three of the measured immune traits. Innate immune function was independent of age and manipulated natal brood size. Our finding that food availability affects innate immune function suggests that fitness effects of food availability may at least partially be mediated by effects on the immune system. However, food availability effects on innate immunity varied in direction between traits, illustrating the complexity of the immune system and precluding conclusions on the level of disease resistance. This paper explores the effects of an ecologically relevant manipulation of foraging effort on a broad array of six innate immune measures, while also looking at effects of development, season and sex.</description><identifier>ISSN: 0021-8790</identifier><identifier>ISSN: 1365-2656</identifier><identifier>EISSN: 1365-2656</identifier><identifier>DOI: 10.1111/1365-2656.13822</identifier><identifier>PMID: 36268692</identifier><language>eng</language><publisher>England: Blackwell Publishing Ltd</publisher><subject>Agglutination ; Animals ; Antibodies ; Availability ; Conalbumin ; Costs ; Disease resistance ; E coli ; Ecophysiology ; Environmental factors ; Escherichia coli ; Food ; Food availability ; Foraging behavior ; foraging effort ; Haptoglobin ; Immune response ; Immune system ; Immunity ; Innate immunity ; Life History Ecology ; Lysis ; Males ; manipulation of food availability ; meso‐population ; Nitric Oxide ; Resource allocation ; Seasonal variations ; zebra finch</subject><ispartof>The Journal of animal ecology, 2022-12, Vol.91 (12), p.2400-2411</ispartof><rights>2022 The Authors. published by John Wiley &amp; Sons Ltd on behalf of British Ecological Society.</rights><rights>2022 The Authors. Journal of Animal Ecology published by John Wiley &amp; Sons Ltd on behalf of British Ecological Society.</rights><rights>2022. This article is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c4232-93b6704ac77f1be4cc9c21a2b6245be1d26915836859ee1c90fa7ad9aa5541073</cites><orcidid>0000-0002-1784-0642 ; 0000-0002-9002-4000 ; 0000-0003-4334-4359 ; 0000-0002-1143-6868 ; 0000-0003-2512-378X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,780,784,885,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/36268692$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Driessen, Merijn M. G.</creatorcontrib><creatorcontrib>Versteegh, Maaike A.</creatorcontrib><creatorcontrib>Gerritsma, Yoran H.</creatorcontrib><creatorcontrib>Tieleman, B. Irene</creatorcontrib><creatorcontrib>Pen, Ido R.</creatorcontrib><creatorcontrib>Verhulst, Simon</creatorcontrib><title>Effects of manipulated food availability and seasonality on innate immune function in a passerine</title><title>The Journal of animal ecology</title><addtitle>J Anim Ecol</addtitle><description>The innate immune system is essential for survival, yet many immune traits are highly variable between and within individuals. In recent years, attention has shifted to the role of environmental factors in modulating this variation. A key environmental factor is food availability, which plays a major role in shaping life histories, and may affect resource allocation to immune function through its effect on nutritional state. We developed a technique to permanently increase foraging costs in seed‐eating birds, and leveraged this technique to study the effects of food availability on the innate immune system over a 3‐year period in 230 zebra finches housed in outdoor aviaries. The immune components we studied were haptoglobin, ovotransferrin, nitric oxide, natural antibodies through agglutination, complement‐mediated lysis, and killing capacity of Escherichia coli and Candida albicans, covering a broad spectrum of the innate immune system. We explored the effects of food availability in conjunction with other potentially important variables: season, age, sex and manipulated natal brood size. Increased foraging costs affected multiple components of the immune system, albeit in a variable way. Nitric oxide and agglutination levels were lower under harsh foraging conditions, while Escherichia coli killing capacity was increased. Agglutination levels also varied seasonally, but only at low foraging costs. C. albicans killing capacity was lower in winter, and even more so for animals in harsh foraging conditions that were raised in large broods. Effects of food availability on ovotransferrin were also seasonal, and only apparent in males. Haptoglobin levels were independent of foraging costs and season. Males had higher levels of immune function than females for three of the measured immune traits. Innate immune function was independent of age and manipulated natal brood size. Our finding that food availability affects innate immune function suggests that fitness effects of food availability may at least partially be mediated by effects on the immune system. However, food availability effects on innate immunity varied in direction between traits, illustrating the complexity of the immune system and precluding conclusions on the level of disease resistance. This paper explores the effects of an ecologically relevant manipulation of foraging effort on a broad array of six innate immune measures, while also looking at effects of development, season and sex.</description><subject>Agglutination</subject><subject>Animals</subject><subject>Antibodies</subject><subject>Availability</subject><subject>Conalbumin</subject><subject>Costs</subject><subject>Disease resistance</subject><subject>E coli</subject><subject>Ecophysiology</subject><subject>Environmental factors</subject><subject>Escherichia coli</subject><subject>Food</subject><subject>Food availability</subject><subject>Foraging behavior</subject><subject>foraging effort</subject><subject>Haptoglobin</subject><subject>Immune response</subject><subject>Immune system</subject><subject>Immunity</subject><subject>Innate immunity</subject><subject>Life History Ecology</subject><subject>Lysis</subject><subject>Males</subject><subject>manipulation of food availability</subject><subject>meso‐population</subject><subject>Nitric Oxide</subject><subject>Resource allocation</subject><subject>Seasonal variations</subject><subject>zebra finch</subject><issn>0021-8790</issn><issn>1365-2656</issn><issn>1365-2656</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><recordid>eNqFkU1v1DAQhi0EotuFMzdkiQuXtP6I7eSEqmopoAoucLYmzhhcJfYSJ6323-PdLSvgwlwsjx-_such5BVnF7zUJZdaVUIrfcFlI8QTsjp1npIVY4JXjWnZGTnP-Y4xZgSTz8mZ1EI3uhUrAhvv0c2ZJk9HiGG7DDBjT31KPYV7CAN0YQjzjkLsaUbIKcJhnyINMRaYhnFcIlK_RDeHQ5sC3ULOOIWIL8gzD0PGl4_rmnx7v_l6_aG6_XLz8frqtnK1kKJqZacNq8EZ43mHtXOtExxEp0WtOuS90C1XjdSNahG5a5kHA30LoFTNmZFr8u6Yu126EXuHcZ5gsNspjDDtbIJg_z6J4Yf9nu4tZ6wVjVAl4e1jwpR-LphnO4bscBggYlqyFUYYXQvFdUHf_IPepWUqk9lTdZlyI0utyeWRclPKeUJ_eg1ndu_P7m3ZvS178FduvP7zEyf-t7AC6CPwEAbc_S_Pfrr6vDkm_wKtAaXk</recordid><startdate>202212</startdate><enddate>202212</enddate><creator>Driessen, Merijn M. G.</creator><creator>Versteegh, Maaike A.</creator><creator>Gerritsma, Yoran H.</creator><creator>Tieleman, B. Irene</creator><creator>Pen, Ido R.</creator><creator>Verhulst, Simon</creator><general>Blackwell Publishing Ltd</general><general>John Wiley and Sons Inc</general><scope>24P</scope><scope>WIN</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QG</scope><scope>7SN</scope><scope>7SS</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-1784-0642</orcidid><orcidid>https://orcid.org/0000-0002-9002-4000</orcidid><orcidid>https://orcid.org/0000-0003-4334-4359</orcidid><orcidid>https://orcid.org/0000-0002-1143-6868</orcidid><orcidid>https://orcid.org/0000-0003-2512-378X</orcidid></search><sort><creationdate>202212</creationdate><title>Effects of manipulated food availability and seasonality on innate immune function in a passerine</title><author>Driessen, Merijn M. G. ; Versteegh, Maaike A. ; Gerritsma, Yoran H. ; Tieleman, B. Irene ; Pen, Ido R. ; Verhulst, Simon</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4232-93b6704ac77f1be4cc9c21a2b6245be1d26915836859ee1c90fa7ad9aa5541073</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Agglutination</topic><topic>Animals</topic><topic>Antibodies</topic><topic>Availability</topic><topic>Conalbumin</topic><topic>Costs</topic><topic>Disease resistance</topic><topic>E coli</topic><topic>Ecophysiology</topic><topic>Environmental factors</topic><topic>Escherichia coli</topic><topic>Food</topic><topic>Food availability</topic><topic>Foraging behavior</topic><topic>foraging effort</topic><topic>Haptoglobin</topic><topic>Immune response</topic><topic>Immune system</topic><topic>Immunity</topic><topic>Innate immunity</topic><topic>Life History Ecology</topic><topic>Lysis</topic><topic>Males</topic><topic>manipulation of food availability</topic><topic>meso‐population</topic><topic>Nitric Oxide</topic><topic>Resource allocation</topic><topic>Seasonal variations</topic><topic>zebra finch</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Driessen, Merijn M. G.</creatorcontrib><creatorcontrib>Versteegh, Maaike A.</creatorcontrib><creatorcontrib>Gerritsma, Yoran H.</creatorcontrib><creatorcontrib>Tieleman, B. Irene</creatorcontrib><creatorcontrib>Pen, Ido R.</creatorcontrib><creatorcontrib>Verhulst, Simon</creatorcontrib><collection>Wiley Online Library Open Access</collection><collection>Wiley Online Library Free Content</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Animal Behavior Abstracts</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The Journal of animal ecology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Driessen, Merijn M. G.</au><au>Versteegh, Maaike A.</au><au>Gerritsma, Yoran H.</au><au>Tieleman, B. Irene</au><au>Pen, Ido R.</au><au>Verhulst, Simon</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Effects of manipulated food availability and seasonality on innate immune function in a passerine</atitle><jtitle>The Journal of animal ecology</jtitle><addtitle>J Anim Ecol</addtitle><date>2022-12</date><risdate>2022</risdate><volume>91</volume><issue>12</issue><spage>2400</spage><epage>2411</epage><pages>2400-2411</pages><issn>0021-8790</issn><issn>1365-2656</issn><eissn>1365-2656</eissn><abstract>The innate immune system is essential for survival, yet many immune traits are highly variable between and within individuals. In recent years, attention has shifted to the role of environmental factors in modulating this variation. A key environmental factor is food availability, which plays a major role in shaping life histories, and may affect resource allocation to immune function through its effect on nutritional state. We developed a technique to permanently increase foraging costs in seed‐eating birds, and leveraged this technique to study the effects of food availability on the innate immune system over a 3‐year period in 230 zebra finches housed in outdoor aviaries. The immune components we studied were haptoglobin, ovotransferrin, nitric oxide, natural antibodies through agglutination, complement‐mediated lysis, and killing capacity of Escherichia coli and Candida albicans, covering a broad spectrum of the innate immune system. We explored the effects of food availability in conjunction with other potentially important variables: season, age, sex and manipulated natal brood size. Increased foraging costs affected multiple components of the immune system, albeit in a variable way. Nitric oxide and agglutination levels were lower under harsh foraging conditions, while Escherichia coli killing capacity was increased. Agglutination levels also varied seasonally, but only at low foraging costs. C. albicans killing capacity was lower in winter, and even more so for animals in harsh foraging conditions that were raised in large broods. Effects of food availability on ovotransferrin were also seasonal, and only apparent in males. Haptoglobin levels were independent of foraging costs and season. Males had higher levels of immune function than females for three of the measured immune traits. Innate immune function was independent of age and manipulated natal brood size. Our finding that food availability affects innate immune function suggests that fitness effects of food availability may at least partially be mediated by effects on the immune system. However, food availability effects on innate immunity varied in direction between traits, illustrating the complexity of the immune system and precluding conclusions on the level of disease resistance. This paper explores the effects of an ecologically relevant manipulation of foraging effort on a broad array of six innate immune measures, while also looking at effects of development, season and sex.</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>36268692</pmid><doi>10.1111/1365-2656.13822</doi><tpages>12</tpages><orcidid>https://orcid.org/0000-0002-1784-0642</orcidid><orcidid>https://orcid.org/0000-0002-9002-4000</orcidid><orcidid>https://orcid.org/0000-0003-4334-4359</orcidid><orcidid>https://orcid.org/0000-0002-1143-6868</orcidid><orcidid>https://orcid.org/0000-0003-2512-378X</orcidid><oa>free_for_read</oa></addata></record>
fulltext fulltext
identifier ISSN: 0021-8790
ispartof The Journal of animal ecology, 2022-12, Vol.91 (12), p.2400-2411
issn 0021-8790
1365-2656
1365-2656
language eng
recordid cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_10092825
source Wiley
subjects Agglutination
Animals
Antibodies
Availability
Conalbumin
Costs
Disease resistance
E coli
Ecophysiology
Environmental factors
Escherichia coli
Food
Food availability
Foraging behavior
foraging effort
Haptoglobin
Immune response
Immune system
Immunity
Innate immunity
Life History Ecology
Lysis
Males
manipulation of food availability
meso‐population
Nitric Oxide
Resource allocation
Seasonal variations
zebra finch
title Effects of manipulated food availability and seasonality on innate immune function in a passerine
url http://sfxeu10.hosted.exlibrisgroup.com/loughborough?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-08T03%3A06%3A50IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Effects%20of%20manipulated%20food%20availability%20and%20seasonality%20on%20innate%20immune%20function%20in%20a%20passerine&rft.jtitle=The%20Journal%20of%20animal%20ecology&rft.au=Driessen,%20Merijn%20M.%20G.&rft.date=2022-12&rft.volume=91&rft.issue=12&rft.spage=2400&rft.epage=2411&rft.pages=2400-2411&rft.issn=0021-8790&rft.eissn=1365-2656&rft_id=info:doi/10.1111/1365-2656.13822&rft_dat=%3Cproquest_pubme%3E2727642516%3C/proquest_pubme%3E%3Cgrp_id%3Ecdi_FETCH-LOGICAL-c4232-93b6704ac77f1be4cc9c21a2b6245be1d26915836859ee1c90fa7ad9aa5541073%3C/grp_id%3E%3Coa%3E%3C/oa%3E%3Curl%3E%3C/url%3E&rft_id=info:oai/&rft_pqid=2747208333&rft_id=info:pmid/36268692&rfr_iscdi=true