Embryonic learning and developmental carry-over effects in an invasive anuran

Carry-over effects influence trait responses in later life stages as a result of early experience with environmental cues. Predation risk is an influential stressor and selection exists for early recognition of threats. In particular, invasive species may benefit from carry-over effects by preemptiv...

Ausführliche Beschreibung

Gespeichert in:
Bibliographische Detailangaben
Veröffentlicht in:Oecologia 2017-07, Vol.184 (3), p.623-631
Hauptverfasser: Garcia, Tiffany S., Urbina, Jenny C., Bredeweg, Evan M., Ferrari, Maud C. O.
Format: Artikel
Sprache:eng
Schlagworte:
Online-Zugang:Volltext
Tags: Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
container_end_page 631
container_issue 3
container_start_page 623
container_title Oecologia
container_volume 184
creator Garcia, Tiffany S.
Urbina, Jenny C.
Bredeweg, Evan M.
Ferrari, Maud C. O.
description Carry-over effects influence trait responses in later life stages as a result of early experience with environmental cues. Predation risk is an influential stressor and selection exists for early recognition of threats. In particular, invasive species may benefit from carry-over effects by preemptively recognizing and responding to novel predators via latent developmental changes and embryonic learning. In a factorial experiment, we conditioned invasive American bullfrog embryos (Lithobates catesbeianus) to the odor of a novel fish predator, largemouth bass (Micropterus salmoides) alone or in combination with injured conspecific cues. We quantified developmental carryover in the larval life stage and found that individuals conditioned to the highest risk (fish and injured conspecific cues) grew into longer bodied larvae relative to larvae from lower risk treatments. We also assessed embryonic learning, a behavioral carry-over effect, and found an interaction between embryonic conditioning and larval exposure. Behavioral responses were only found in scenarios when predation risk varied in intensity across life history stages, thus requiring a more flexible antipredator strategy. This indicates a potential trade-off between the two strategies in larval growth and development rates, and time until metamorphosis. Our results suggest that early predator exposure and carry-over effects have significant impacts on life history trajectories for American bullfrogs. This research contributes to our understanding of a potentially important invasion mechanism in an anuran species of conservation concern.
doi_str_mv 10.1007/s00442-017-3905-5
format Article
fullrecord <record><control><sourceid>gale_proqu</sourceid><recordid>TN_cdi_proquest_miscellaneous_1915556240</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><galeid>A498598690</galeid><jstor_id>48718754</jstor_id><sourcerecordid>A498598690</sourcerecordid><originalsourceid>FETCH-LOGICAL-c495t-328f5dd69f3000c81cb0b53481219561c19fa52e40bef45fbf890bdaaa8055f93</originalsourceid><addsrcrecordid>eNp9kVFrFDEUhYModq3-AB-UAV_0YerNTDKTPJZStVApVH0OmczNkmUmWZOZxf33Zplau0UkkFxyv3PIzSHkNYUzCtB-TACMVSXQtqwl8JI_ISvK6qqkspZPyQqgkqXgTJ6QFyltACijnD8nJ5VoGpm7K_L1cuziPnhnigF19M6vC-37oscdDmE7op_0UBgd474MO4wFWotmSoXzmcv7Tie3w1zPUfuX5JnVQ8JXd-cp-fHp8vvFl_L65vPVxfl1aZjkU1lXwvK-b6StAcAIajroeM0ErajkDTVUWs0rZNChZdx2Vkjoeq21AM6trE_J-8V3G8PPGdOkRpcMDoP2GOakqMxz8qZikNF3j9BNmKPPrztQEtpaMPGXWusBlfM2TFGbg6k6Z1JwKfJ_ZersH1RePY7OBI_W5fsjwYcjQWYm_DWt9ZySuvp2e8zShTUxpBTRqm10o457RUEd4lZL3CrHrQ5xK541b--Gm7sR-3vFn3wzUC1Ayi2_xvhg-v-4vllEmzSFeG_KREtFy1n9G9Jdu34</addsrcrecordid><sourcetype>Aggregation Database</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>1919073848</pqid></control><display><type>article</type><title>Embryonic learning and developmental carry-over effects in an invasive anuran</title><source>Jstor Complete Legacy</source><source>MEDLINE</source><source>SpringerLink Journals</source><creator>Garcia, Tiffany S. ; Urbina, Jenny C. ; Bredeweg, Evan M. ; Ferrari, Maud C. O.</creator><creatorcontrib>Garcia, Tiffany S. ; Urbina, Jenny C. ; Bredeweg, Evan M. ; Ferrari, Maud C. O.</creatorcontrib><description>Carry-over effects influence trait responses in later life stages as a result of early experience with environmental cues. Predation risk is an influential stressor and selection exists for early recognition of threats. In particular, invasive species may benefit from carry-over effects by preemptively recognizing and responding to novel predators via latent developmental changes and embryonic learning. In a factorial experiment, we conditioned invasive American bullfrog embryos (Lithobates catesbeianus) to the odor of a novel fish predator, largemouth bass (Micropterus salmoides) alone or in combination with injured conspecific cues. We quantified developmental carryover in the larval life stage and found that individuals conditioned to the highest risk (fish and injured conspecific cues) grew into longer bodied larvae relative to larvae from lower risk treatments. We also assessed embryonic learning, a behavioral carry-over effect, and found an interaction between embryonic conditioning and larval exposure. Behavioral responses were only found in scenarios when predation risk varied in intensity across life history stages, thus requiring a more flexible antipredator strategy. This indicates a potential trade-off between the two strategies in larval growth and development rates, and time until metamorphosis. Our results suggest that early predator exposure and carry-over effects have significant impacts on life history trajectories for American bullfrogs. This research contributes to our understanding of a potentially important invasion mechanism in an anuran species of conservation concern.</description><identifier>ISSN: 0029-8549</identifier><identifier>EISSN: 1432-1939</identifier><identifier>DOI: 10.1007/s00442-017-3905-5</identifier><identifier>PMID: 28669002</identifier><language>eng</language><publisher>Berlin/Heidelberg: Springer Science + Business Media</publisher><subject>Animals ; Anti-predator behavior ; Anura ; Bass ; BEHAVIORAL ECOLOGY – ORIGINAL RESEARCH ; Biomedical and Life Sciences ; Conditioning ; Cues ; Developmental stages ; Early experience ; Ecology ; Embryonic development ; Embryos ; Exposure ; Fish ; Fishes ; Freshwater fishes ; Hydrology/Water Resources ; Introduced Species ; Invasive fish ; Invasive species ; Larva ; Larvae ; Larval development ; Learning ; Life Cycle Stages ; Life history ; Life Sciences ; Metamorphosis ; Metamorphosis, Biological ; Odor ; Plant Sciences ; Predation ; Predators ; Predatory Behavior ; Wildlife conservation</subject><ispartof>Oecologia, 2017-07, Vol.184 (3), p.623-631</ispartof><rights>Springer-Verlag GmbH Germany 2017</rights><rights>COPYRIGHT 2017 Springer</rights><rights>Oecologia is a copyright of Springer, 2017.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c495t-328f5dd69f3000c81cb0b53481219561c19fa52e40bef45fbf890bdaaa8055f93</citedby><cites>FETCH-LOGICAL-c495t-328f5dd69f3000c81cb0b53481219561c19fa52e40bef45fbf890bdaaa8055f93</cites><orcidid>0000-0002-0590-3482</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/48718754$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/48718754$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>314,776,780,799,27901,27902,41464,42533,51294,57992,58225</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28669002$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Garcia, Tiffany S.</creatorcontrib><creatorcontrib>Urbina, Jenny C.</creatorcontrib><creatorcontrib>Bredeweg, Evan M.</creatorcontrib><creatorcontrib>Ferrari, Maud C. O.</creatorcontrib><title>Embryonic learning and developmental carry-over effects in an invasive anuran</title><title>Oecologia</title><addtitle>Oecologia</addtitle><addtitle>Oecologia</addtitle><description>Carry-over effects influence trait responses in later life stages as a result of early experience with environmental cues. Predation risk is an influential stressor and selection exists for early recognition of threats. In particular, invasive species may benefit from carry-over effects by preemptively recognizing and responding to novel predators via latent developmental changes and embryonic learning. In a factorial experiment, we conditioned invasive American bullfrog embryos (Lithobates catesbeianus) to the odor of a novel fish predator, largemouth bass (Micropterus salmoides) alone or in combination with injured conspecific cues. We quantified developmental carryover in the larval life stage and found that individuals conditioned to the highest risk (fish and injured conspecific cues) grew into longer bodied larvae relative to larvae from lower risk treatments. We also assessed embryonic learning, a behavioral carry-over effect, and found an interaction between embryonic conditioning and larval exposure. Behavioral responses were only found in scenarios when predation risk varied in intensity across life history stages, thus requiring a more flexible antipredator strategy. This indicates a potential trade-off between the two strategies in larval growth and development rates, and time until metamorphosis. Our results suggest that early predator exposure and carry-over effects have significant impacts on life history trajectories for American bullfrogs. This research contributes to our understanding of a potentially important invasion mechanism in an anuran species of conservation concern.</description><subject>Animals</subject><subject>Anti-predator behavior</subject><subject>Anura</subject><subject>Bass</subject><subject>BEHAVIORAL ECOLOGY – ORIGINAL RESEARCH</subject><subject>Biomedical and Life Sciences</subject><subject>Conditioning</subject><subject>Cues</subject><subject>Developmental stages</subject><subject>Early experience</subject><subject>Ecology</subject><subject>Embryonic development</subject><subject>Embryos</subject><subject>Exposure</subject><subject>Fish</subject><subject>Fishes</subject><subject>Freshwater fishes</subject><subject>Hydrology/Water Resources</subject><subject>Introduced Species</subject><subject>Invasive fish</subject><subject>Invasive species</subject><subject>Larva</subject><subject>Larvae</subject><subject>Larval development</subject><subject>Learning</subject><subject>Life Cycle Stages</subject><subject>Life history</subject><subject>Life Sciences</subject><subject>Metamorphosis</subject><subject>Metamorphosis, Biological</subject><subject>Odor</subject><subject>Plant Sciences</subject><subject>Predation</subject><subject>Predators</subject><subject>Predatory Behavior</subject><subject>Wildlife conservation</subject><issn>0029-8549</issn><issn>1432-1939</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><recordid>eNp9kVFrFDEUhYModq3-AB-UAV_0YerNTDKTPJZStVApVH0OmczNkmUmWZOZxf33Zplau0UkkFxyv3PIzSHkNYUzCtB-TACMVSXQtqwl8JI_ISvK6qqkspZPyQqgkqXgTJ6QFyltACijnD8nJ5VoGpm7K_L1cuziPnhnigF19M6vC-37oscdDmE7op_0UBgd474MO4wFWotmSoXzmcv7Tie3w1zPUfuX5JnVQ8JXd-cp-fHp8vvFl_L65vPVxfl1aZjkU1lXwvK-b6StAcAIajroeM0ErajkDTVUWs0rZNChZdx2Vkjoeq21AM6trE_J-8V3G8PPGdOkRpcMDoP2GOakqMxz8qZikNF3j9BNmKPPrztQEtpaMPGXWusBlfM2TFGbg6k6Z1JwKfJ_ZersH1RePY7OBI_W5fsjwYcjQWYm_DWt9ZySuvp2e8zShTUxpBTRqm10o457RUEd4lZL3CrHrQ5xK541b--Gm7sR-3vFn3wzUC1Ayi2_xvhg-v-4vllEmzSFeG_KREtFy1n9G9Jdu34</recordid><startdate>20170701</startdate><enddate>20170701</enddate><creator>Garcia, Tiffany S.</creator><creator>Urbina, Jenny C.</creator><creator>Bredeweg, Evan M.</creator><creator>Ferrari, Maud C. O.</creator><general>Springer Science + Business Media</general><general>Springer Berlin Heidelberg</general><general>Springer</general><general>Springer Nature B.V</general><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>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7SN</scope><scope>7SS</scope><scope>7T7</scope><scope>7TN</scope><scope>7U9</scope><scope>7X7</scope><scope>7XB</scope><scope>88A</scope><scope>88E</scope><scope>8AO</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>BKSAR</scope><scope>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>F1W</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>H95</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>L.G</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>P64</scope><scope>PCBAR</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>RC3</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0002-0590-3482</orcidid></search><sort><creationdate>20170701</creationdate><title>Embryonic learning and developmental carry-over effects in an invasive anuran</title><author>Garcia, Tiffany S. ; Urbina, Jenny C. ; Bredeweg, Evan M. ; Ferrari, Maud C. O.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c495t-328f5dd69f3000c81cb0b53481219561c19fa52e40bef45fbf890bdaaa8055f93</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>Animals</topic><topic>Anti-predator behavior</topic><topic>Anura</topic><topic>Bass</topic><topic>BEHAVIORAL ECOLOGY – ORIGINAL RESEARCH</topic><topic>Biomedical and Life Sciences</topic><topic>Conditioning</topic><topic>Cues</topic><topic>Developmental stages</topic><topic>Early experience</topic><topic>Ecology</topic><topic>Embryonic development</topic><topic>Embryos</topic><topic>Exposure</topic><topic>Fish</topic><topic>Fishes</topic><topic>Freshwater fishes</topic><topic>Hydrology/Water Resources</topic><topic>Introduced Species</topic><topic>Invasive fish</topic><topic>Invasive species</topic><topic>Larva</topic><topic>Larvae</topic><topic>Larval development</topic><topic>Learning</topic><topic>Life Cycle Stages</topic><topic>Life history</topic><topic>Life Sciences</topic><topic>Metamorphosis</topic><topic>Metamorphosis, Biological</topic><topic>Odor</topic><topic>Plant Sciences</topic><topic>Predation</topic><topic>Predators</topic><topic>Predatory Behavior</topic><topic>Wildlife conservation</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Garcia, Tiffany S.</creatorcontrib><creatorcontrib>Urbina, Jenny C.</creatorcontrib><creatorcontrib>Bredeweg, Evan M.</creatorcontrib><creatorcontrib>Ferrari, Maud C. O.</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Science</collection><collection>ProQuest Central (Corporate)</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Oceanic Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Health &amp; Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Biology Database (Alumni Edition)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest One Sustainability</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>Earth, Atmospheric &amp; Aquatic Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>ASFA: Aquatic Sciences and Fisheries Abstracts</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Aquatic Science &amp; Fisheries Abstracts (ASFA) 1: Biological Sciences &amp; Living Resources</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health &amp; Medical Complete (Alumni)</collection><collection>Aquatic Science &amp; Fisheries Abstracts (ASFA) Professional</collection><collection>ProQuest Biological Science Collection</collection><collection>Health &amp; Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biological Science Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Earth, Atmospheric &amp; Aquatic Science Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Oecologia</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Garcia, Tiffany S.</au><au>Urbina, Jenny C.</au><au>Bredeweg, Evan M.</au><au>Ferrari, Maud C. O.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Embryonic learning and developmental carry-over effects in an invasive anuran</atitle><jtitle>Oecologia</jtitle><stitle>Oecologia</stitle><addtitle>Oecologia</addtitle><date>2017-07-01</date><risdate>2017</risdate><volume>184</volume><issue>3</issue><spage>623</spage><epage>631</epage><pages>623-631</pages><issn>0029-8549</issn><eissn>1432-1939</eissn><abstract>Carry-over effects influence trait responses in later life stages as a result of early experience with environmental cues. Predation risk is an influential stressor and selection exists for early recognition of threats. In particular, invasive species may benefit from carry-over effects by preemptively recognizing and responding to novel predators via latent developmental changes and embryonic learning. In a factorial experiment, we conditioned invasive American bullfrog embryos (Lithobates catesbeianus) to the odor of a novel fish predator, largemouth bass (Micropterus salmoides) alone or in combination with injured conspecific cues. We quantified developmental carryover in the larval life stage and found that individuals conditioned to the highest risk (fish and injured conspecific cues) grew into longer bodied larvae relative to larvae from lower risk treatments. We also assessed embryonic learning, a behavioral carry-over effect, and found an interaction between embryonic conditioning and larval exposure. Behavioral responses were only found in scenarios when predation risk varied in intensity across life history stages, thus requiring a more flexible antipredator strategy. This indicates a potential trade-off between the two strategies in larval growth and development rates, and time until metamorphosis. Our results suggest that early predator exposure and carry-over effects have significant impacts on life history trajectories for American bullfrogs. This research contributes to our understanding of a potentially important invasion mechanism in an anuran species of conservation concern.</abstract><cop>Berlin/Heidelberg</cop><pub>Springer Science + Business Media</pub><pmid>28669002</pmid><doi>10.1007/s00442-017-3905-5</doi><tpages>9</tpages><orcidid>https://orcid.org/0000-0002-0590-3482</orcidid></addata></record>
fulltext fulltext
identifier ISSN: 0029-8549
ispartof Oecologia, 2017-07, Vol.184 (3), p.623-631
issn 0029-8549
1432-1939
language eng
recordid cdi_proquest_miscellaneous_1915556240
source Jstor Complete Legacy; MEDLINE; SpringerLink Journals
subjects Animals
Anti-predator behavior
Anura
Bass
BEHAVIORAL ECOLOGY – ORIGINAL RESEARCH
Biomedical and Life Sciences
Conditioning
Cues
Developmental stages
Early experience
Ecology
Embryonic development
Embryos
Exposure
Fish
Fishes
Freshwater fishes
Hydrology/Water Resources
Introduced Species
Invasive fish
Invasive species
Larva
Larvae
Larval development
Learning
Life Cycle Stages
Life history
Life Sciences
Metamorphosis
Metamorphosis, Biological
Odor
Plant Sciences
Predation
Predators
Predatory Behavior
Wildlife conservation
title Embryonic learning and developmental carry-over effects in an invasive anuran
url https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-03T09%3A13%3A39IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_proqu&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Embryonic%20learning%20and%20developmental%20carry-over%20effects%20in%20an%20invasive%20anuran&rft.jtitle=Oecologia&rft.au=Garcia,%20Tiffany%20S.&rft.date=2017-07-01&rft.volume=184&rft.issue=3&rft.spage=623&rft.epage=631&rft.pages=623-631&rft.issn=0029-8549&rft.eissn=1432-1939&rft_id=info:doi/10.1007/s00442-017-3905-5&rft_dat=%3Cgale_proqu%3EA498598690%3C/gale_proqu%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1919073848&rft_id=info:pmid/28669002&rft_galeid=A498598690&rft_jstor_id=48718754&rfr_iscdi=true