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...
Saved in:
Published in: | The Journal of animal ecology 2022-12, Vol.91 (12), p.2400-2411 |
---|---|
Main Authors: | , , , , , |
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 & Sons Ltd on behalf of British Ecological Society.</rights><rights>2022 The Authors. Journal of Animal Ecology published by John Wiley & 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 |