Intensified agriculture favors evolved resistance to biological control

Increased regulation of chemical pesticides and rapid evolution of pesticide resistance have increased calls for sustainable pest management. Biological control offers sustainable pest suppression, partly because evolution of resistance to predators and parasitoids is prevented by several factors (e...

Full description

Saved in:
Bibliographic Details
Published inProceedings of the National Academy of Sciences - PNAS Vol. 114; no. 15; pp. 3885 - 3890
Main Authors Tomasetto, Federico, Tylianakis, Jason M., Reale, Marco, Wratten, Steve, Goldson, Stephen L.
Format Journal Article
LanguageEnglish
Published United States National Academy of Sciences 11.04.2017
SeriesFrom the Cover
Subjects
Online AccessGet full text
ISSN0027-8424
1091-6490
1091-6490
DOI10.1073/pnas.1618416114

Cover

Loading…
Abstract Increased regulation of chemical pesticides and rapid evolution of pesticide resistance have increased calls for sustainable pest management. Biological control offers sustainable pest suppression, partly because evolution of resistance to predators and parasitoids is prevented by several factors (e.g., spatial or temporal refuges from attacks, reciprocal evolution by control agents, and contrasting selection pressures from other enemy species). However, evolution of resistance may become more probable as agricultural intensification reduces the availability of refuges and diversity of enemy species, or if control agents have genetic barriers to evolution. Here we use 21 y of field data from 196 sites across New Zealand to show that parasitism of a key pasture pest (Listronotus bonariensis; Argentine stem weevil) by an introduced parasitoid (Microctonus hyperodae) was initially nationally successful but then declined by 44% (leading to pasture damage of c. 160 million New Zealand dollars per annum). This decline was not attributable to parasitoid numbers released, elevation, or local climatic variables at sample locations. Rather, in all locations the decline began 7 y (14 host generations) following parasitoid introduction, despite releases being staggered across locations in different years. Finally, we demonstrate experimentally that declining parasitism rates occurred in ryegrass Lolium perenne, which is grown nationwide in high-intensity was significantly less than in adjacent plots of a less-common pasture grass (Lolium multiflorum), indicating that resistance to parasitism is host plant–dependent. We conclude that low plant and enemy biodiversity in intensive large-scale agriculture may facilitate the evolution of host resistance by pests and threaten the long-term viability of biological control.
AbstractList Increased regulation of chemical pesticides and rapid evolution of pesticide resistance have increased calls for sustainable pest management. Biological control offers sustainable pest suppression, partly because evolution of resistance to predators and parasitoids is prevented by several factors (e.g., spatial or temporal refuges from attacks, reciprocal evolution by control agents, and contrasting selection pressures from other enemy species). However, evolution of resistance may become more probable as agricultural intensification reduces the availability of refuges and diversity of enemy species, or if control agents have genetic barriers to evolution. Here we use 21 y of field data from 196 sites across New Zealand to show that parasitism of a key pasture pest (Listronotus bonariensis; Argentine stem weevil) by an introduced parasitoid (Microctonus hyperodae) was initially nationally successful but then declined by 44% (leading to pasture damage of c. 160 million New Zealand dollars per annum). This decline was not attributable to parasitoid numbers released, elevation, or local climatic variables at sample locations. Rather, in all locations the decline began 7 y (14 host generations) following parasitoid introduction, despite releases being staggered across locations in different years. Finally, we demonstrate experimentally that declining parasitism rates occurred in ryegrass Lolium perenne, which is grown nationwide in high-intensity was significantly less than in adjacent plots of a less-common pasture grass (Lolium multiflorum), indicating that resistance to parasitism is host plant-dependent. We conclude that low plant and enemy biodiversity in intensive large-scale agriculture may facilitate the evolution of host resistance by pests and threaten the long-term viability of biological control.
The need for agricultural production to meet the food demands of a growing human population will require sustainable and acceptable pest management, such as biological control, across 11% (1.5 billion ha) of the globe’s land surface. However, the long-term viability of this ecosystem service can be threatened by the expansion and simplification of agricultural systems, which may facilitate the evolution of resistance by pests to their control agents. This study uses a national dataset to present evidence for the acquisition of resistance by a ryegrass weevil pest to its parasitoid wasp over the last 21 y. This resistance was not associated with differences in environmental conditions but rather is specific to the most commonly grown pasture grass species. Increased regulation of chemical pesticides and rapid evolution of pesticide resistance have increased calls for sustainable pest management. Biological control offers sustainable pest suppression, partly because evolution of resistance to predators and parasitoids is prevented by several factors (e.g., spatial or temporal refuges from attacks, reciprocal evolution by control agents, and contrasting selection pressures from other enemy species). However, evolution of resistance may become more probable as agricultural intensification reduces the availability of refuges and diversity of enemy species, or if control agents have genetic barriers to evolution. Here we use 21 y of field data from 196 sites across New Zealand to show that parasitism of a key pasture pest ( Listronotus bonariensis ; Argentine stem weevil) by an introduced parasitoid ( Microctonus hyperodae ) was initially nationally successful but then declined by 44% (leading to pasture damage of c. 160 million New Zealand dollars per annum). This decline was not attributable to parasitoid numbers released, elevation, or local climatic variables at sample locations. Rather, in all locations the decline began 7 y (14 host generations) following parasitoid introduction, despite releases being staggered across locations in different years. Finally, we demonstrate experimentally that declining parasitism rates occurred in ryegrass Lolium perenne , which is grown nationwide in high-intensity was significantly less than in adjacent plots of a less-common pasture grass ( Lolium multiflorum ), indicating that resistance to parasitism is host plant–dependent. We conclude that low plant and enemy biodiversity in intensive large-scale agriculture may facilitate the evolution of host resistance by pests and threaten the long-term viability of biological control.
Increased regulation of chemical pesticides and rapid evolution of pesticide resistance have increased calls for sustainable pest management. Biological control offers sustainable pest suppression, partly because evolution of resistance to predators and parasitoids is prevented by several factors (e.g., spatial or temporal refuges from attacks, reciprocal evolution by control agents, and contrasting selection pressures from other enemy species). However, evolution of resistance may become more probable as agricultural intensification reduces the availability of refuges and diversity of enemy species, or if control agents have genetic barriers to evolution. Here we use 21 y of field data from 196 sites across New Zealand to show that parasitism of a key pasture pest ( ; Argentine stem weevil) by an introduced parasitoid ( ) was initially nationally successful but then declined by 44% (leading to pasture damage of c. 160 million New Zealand dollars per annum). This decline was not attributable to parasitoid numbers released, elevation, or local climatic variables at sample locations. Rather, in all locations the decline began 7 y (14 host generations) following parasitoid introduction, despite releases being staggered across locations in different years. Finally, we demonstrate experimentally that declining parasitism rates occurred in ryegrass , which is grown nationwide in high-intensity was significantly less than in adjacent plots of a less-common pasture grass ( ), indicating that resistance to parasitism is host plant-dependent. We conclude that low plant and enemy biodiversity in intensive large-scale agriculture may facilitate the evolution of host resistance by pests and threaten the long-term viability of biological control.
Increased regulation of chemical pesticides and rapid evolution of pesticide resistance have increased calls for sustainable pest management. Biological control offers sustainable pest suppression, partly because evolution of resistance to predators and parasitoids is prevented by several factors (e.g., spatial or temporal refuges from attacks, reciprocal evolution by control agents, and contrasting selection pressures from other enemy species). However, evolution of resistance may become more probable as agricultural intensification reduces the availability of refuges and diversity of enemy species, or if control agents have genetic barriers to evolution. Here we use 21 y of field data from 196 sites across New Zealand to show that parasitism of a key pasture pest (Listronotus bonariensis; Argentine stem weevil) by an introduced parasitoid (Microctonus hyperodae) was initially nationally successful but then declined by 44% (leading to pasture damage of c. 160 million New Zealand dollars per annum). This decline was not attributable to parasitoid numbers released, elevation, or local climatic variables at sample locations. Rather, in all locations the decline began 7 y (14 host generations) following parasitoid introduction, despite releases being staggered across locations in different years. Finally, we demonstrate experimentally that declining parasitism rates occurred in ryegrass Lolium perenne, which is grown nationwide in high-intensity was significantly less than in adjacent plots of a less-common pasture grass (Lolium multiflorum), indicating that resistance to parasitism is host plant-dependent. We conclude that low plant and enemy biodiversity in intensive large-scale agriculture may facilitate the evolution of host resistance by pests and threaten the long-term viability of biological control.Increased regulation of chemical pesticides and rapid evolution of pesticide resistance have increased calls for sustainable pest management. Biological control offers sustainable pest suppression, partly because evolution of resistance to predators and parasitoids is prevented by several factors (e.g., spatial or temporal refuges from attacks, reciprocal evolution by control agents, and contrasting selection pressures from other enemy species). However, evolution of resistance may become more probable as agricultural intensification reduces the availability of refuges and diversity of enemy species, or if control agents have genetic barriers to evolution. Here we use 21 y of field data from 196 sites across New Zealand to show that parasitism of a key pasture pest (Listronotus bonariensis; Argentine stem weevil) by an introduced parasitoid (Microctonus hyperodae) was initially nationally successful but then declined by 44% (leading to pasture damage of c. 160 million New Zealand dollars per annum). This decline was not attributable to parasitoid numbers released, elevation, or local climatic variables at sample locations. Rather, in all locations the decline began 7 y (14 host generations) following parasitoid introduction, despite releases being staggered across locations in different years. Finally, we demonstrate experimentally that declining parasitism rates occurred in ryegrass Lolium perenne, which is grown nationwide in high-intensity was significantly less than in adjacent plots of a less-common pasture grass (Lolium multiflorum), indicating that resistance to parasitism is host plant-dependent. We conclude that low plant and enemy biodiversity in intensive large-scale agriculture may facilitate the evolution of host resistance by pests and threaten the long-term viability of biological control.
Author Goldson, Stephen L.
Tylianakis, Jason M.
Reale, Marco
Tomasetto, Federico
Wratten, Steve
Author_xml – sequence: 1
  givenname: Federico
  surname: Tomasetto
  fullname: Tomasetto, Federico
  organization: AgResearch Ltd., Christchurch 8140, New Zealand
– sequence: 2
  givenname: Jason M.
  surname: Tylianakis
  fullname: Tylianakis, Jason M.
  organization: Department of Life Sciences, Imperial College London, Silwood Park Campus, Ascot, Berkshire SL5 7PY, United Kingdom
– sequence: 3
  givenname: Marco
  surname: Reale
  fullname: Reale, Marco
  organization: School of Mathematics and Statistics, University of Canterbury, Christchurch 8140, New Zealand
– sequence: 4
  givenname: Steve
  surname: Wratten
  fullname: Wratten, Steve
  organization: Bio-Protection Research Centre, Lincoln University, Lincoln 7647, New Zealand
– sequence: 5
  givenname: Stephen L.
  surname: Goldson
  fullname: Goldson, Stephen L.
  organization: Bio-Protection Research Centre, Lincoln University, Lincoln 7647, New Zealand
BackLink https://www.ncbi.nlm.nih.gov/pubmed/28289202$$D View this record in MEDLINE/PubMed
BookMark eNp1UU1PGzEUtCqqEtKeewKt1Esvgedv7wWpQi0gIXGhZ8vreFNHjh1sb6T--zoKlILUy_Phzcwbz5ygo5iiQ-gzhnMMkl5soynnWGDF2sDsHZph6PFCsB6O0AyAyIVihB2jk1LWANBzBR_QMVFE9QTIDF3fxupi8aN3y86ssrdTqFN23Wh2KZfO7VLYtVV2xZdqonVdTd3gU0grb03obIo1p_ARvR9NKO7T0ztHP398f7i6WdzdX99efbtbWA59bVMqR0Y7KI6JUAoLAdgS6QZuzLgEozDmltCBD8zKtsYSjwYMXwqnGACdo8uD7nYaNm5pXbtugt5mvzH5t07G69eb6H_pVdppTntKWmRz9PVJIKfHyZWqN75YF4KJLk1FYyUlJxKL_a0vb6DrNOXYvtdQveipYpw01Nm_jv5aec64AfgBYHMqJbtRW19N9fvgjA8ag953qfdd6pcuG-_iDe9Z-v-M0wNjXWrKL04EU6AopX8AXZSriQ
CitedBy_id crossref_primary_10_1007_s10526_021_10104_8
crossref_primary_10_1111_een_13014
crossref_primary_10_1093_jisesa_ieaa018
crossref_primary_10_1007_s10340_019_01156_y
crossref_primary_10_1016_j_agee_2023_108345
crossref_primary_10_1111_1365_2664_14608
crossref_primary_10_1073_pnas_1702753114
crossref_primary_10_3389_fsufs_2022_1021861
crossref_primary_10_1080_00288233_2023_2211776
crossref_primary_10_1016_j_scitotenv_2019_01_077
crossref_primary_10_1016_j_ibmb_2022_103897
crossref_primary_10_3389_fevo_2024_1470023
crossref_primary_10_1038_s41559_020_1155_0
crossref_primary_10_1002_ece3_3667
crossref_primary_10_1093_jisesa_iez085
crossref_primary_10_3390_land11010083
crossref_primary_10_1111_aen_12640
crossref_primary_10_1093_bib_bbab205
crossref_primary_10_1111_tpj_13773
crossref_primary_10_1007_s42360_021_00334_2
crossref_primary_10_1111_eva_12934
crossref_primary_10_2135_cropsci2017_05_0317
crossref_primary_10_1007_s10526_018_9878_4
crossref_primary_10_1002_evl3_148
crossref_primary_10_1007_s11829_023_10027_4
crossref_primary_10_1038_s41559_020_1184_8
crossref_primary_10_1111_eva_13067
crossref_primary_10_48130_fia_0024_0014
crossref_primary_10_1016_j_ijheh_2020_113486
crossref_primary_10_2108_zs190067
crossref_primary_10_3389_fpls_2017_01413
crossref_primary_10_3390_insects11070441
crossref_primary_10_1007_s10526_020_10027_w
crossref_primary_10_3389_fpls_2022_923237
crossref_primary_10_1080_00288233_2023_2294783
crossref_primary_10_1080_03036758_2017_1385030
crossref_primary_10_1016_j_cois_2018_01_011
crossref_primary_10_1093_gbe_evac030
crossref_primary_10_1080_03036758_2021_2008985
crossref_primary_10_1016_j_tree_2024_04_002
crossref_primary_10_1111_eva_13255
crossref_primary_10_1111_afe_12353
crossref_primary_10_1016_j_agee_2019_106682
crossref_primary_10_1111_raq_12528
crossref_primary_10_1007_s10530_020_02375_6
crossref_primary_10_3389_fevo_2022_923248
crossref_primary_10_1080_00218839_2020_1828237
crossref_primary_10_1186_s12864_023_09538_4
crossref_primary_10_1186_s12864_024_10215_3
crossref_primary_10_1007_s10526_020_10037_8
crossref_primary_10_1007_s13744_023_01097_3
crossref_primary_10_1111_mec_14879
crossref_primary_10_1016_j_gloenvcha_2024_102802
crossref_primary_10_1186_s43170_024_00273_8
crossref_primary_10_2989_20702620_2020_1813651
crossref_primary_10_1016_j_agee_2022_108157
crossref_primary_10_1016_j_biocontrol_2022_104875
crossref_primary_10_1016_j_tree_2023_01_012
crossref_primary_10_1371_journal_pone_0207610
crossref_primary_10_1016_j_biocontrol_2019_01_014
crossref_primary_10_1016_j_ijpara_2020_05_009
crossref_primary_10_3390_agriculture11010016
crossref_primary_10_1007_s10526_024_10275_0
crossref_primary_10_1016_j_biocontrol_2024_105680
crossref_primary_10_1080_00288233_2022_2084121
crossref_primary_10_3390_insects9040131
crossref_primary_10_1098_rspb_2019_1676
crossref_primary_10_3389_fevo_2018_00215
Cites_doi 10.1002/jae.659
10.1126/science.291.5511.2141
10.1093/biomet/65.2.297
10.1086/283012
10.1080/00288230809510453
10.1111/j.1461-0248.2008.01250.x
10.2307/2951597
10.2307/1311994
10.1079/9780851993232.0000
10.1007/BF02373087
10.1641/0006-3568(2006)56[311:TEVOES]2.0.CO;2
10.2307/5485
10.1146/annurev.en.36.010191.003021
10.1146/annurev.en.39.010194.000403
10.1093/ee/27.6.1386
10.1016/j.biocontrol.2007.08.006
10.3389/fpls.2016.01259
10.1093/jee/99.2.273
10.1016/0167-8809(89)90021-2
10.1016/j.cois.2014.09.003
10.1017/S0007485300042152
10.1146/annurev.ento.45.1.175
10.1080/03014223.1998.9518148
10.1126/science.231.4743.1255
10.1016/S0169-5347(97)87378-8
10.1007/BF02373133
10.1007/s004420100716
10.1126/science.1057544
10.1098/rstb.1988.0001
10.1126/science.1206360
10.1111/j.1461-0248.2006.00922.x
10.1007/BF01237660
10.1146/annurev.en.36.010191.002413
10.1007/s10905-005-5614-x
10.1016/S1049-9644(02)00018-X
10.1016/j.cub.2014.04.053
10.1080/03014223.2013.794847
10.2307/5577
10.1080/03014223.1981.10427942
10.1890/0012-9658(1997)078[1673:WIBCES]2.0.CO;2
10.1126/science.1185383
10.1038/38483
10.1038/ncomms12986
10.1038/35015069
10.1038/nature01014
10.1016/j.biocontrol.2014.02.012
10.1086/282265
10.1111/j.1752-4571.2010.00166.x
10.1080/09583159409355347
ContentType Journal Article
Copyright Volumes 1–89 and 106–114, copyright as a collective work only; author(s) retains copyright to individual articles
Copyright National Academy of Sciences Apr 11, 2017
Copyright_xml – notice: Volumes 1–89 and 106–114, copyright as a collective work only; author(s) retains copyright to individual articles
– notice: Copyright National Academy of Sciences Apr 11, 2017
DBID AAYXX
CITATION
CGR
CUY
CVF
ECM
EIF
NPM
7QG
7QL
7QP
7QR
7SN
7SS
7T5
7TK
7TM
7TO
7U9
8FD
C1K
FR3
H94
M7N
P64
RC3
7X8
5PM
DOI 10.1073/pnas.1618416114
DatabaseName CrossRef
Medline
MEDLINE
MEDLINE (Ovid)
MEDLINE
MEDLINE
PubMed
Animal Behavior Abstracts
Bacteriology Abstracts (Microbiology B)
Calcium & Calcified Tissue Abstracts
Chemoreception Abstracts
Ecology Abstracts
Entomology Abstracts (Full archive)
Immunology Abstracts
Neurosciences Abstracts
Nucleic Acids Abstracts
Oncogenes and Growth Factors Abstracts
Virology and AIDS Abstracts
Technology Research Database
Environmental Sciences and Pollution Management
Engineering Research Database
AIDS and Cancer Research Abstracts
Algology Mycology and Protozoology Abstracts (Microbiology C)
Biotechnology and BioEngineering Abstracts
Genetics Abstracts
MEDLINE - Academic
PubMed Central (Full Participant titles)
DatabaseTitle CrossRef
MEDLINE
Medline Complete
MEDLINE with Full Text
PubMed
MEDLINE (Ovid)
Virology and AIDS Abstracts
Oncogenes and Growth Factors Abstracts
Technology Research Database
Nucleic Acids Abstracts
Ecology Abstracts
Neurosciences Abstracts
Biotechnology and BioEngineering Abstracts
Environmental Sciences and Pollution Management
Entomology Abstracts
Genetics Abstracts
Animal Behavior Abstracts
Bacteriology Abstracts (Microbiology B)
Algology Mycology and Protozoology Abstracts (Microbiology C)
AIDS and Cancer Research Abstracts
Chemoreception Abstracts
Immunology Abstracts
Engineering Research Database
Calcium & Calcified Tissue Abstracts
MEDLINE - Academic
DatabaseTitleList Virology and AIDS Abstracts

CrossRef
MEDLINE
MEDLINE - Academic

Database_xml – sequence: 1
  dbid: NPM
  name: PubMed
  url: https://proxy.k.utb.cz/login?url=http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed
  sourceTypes: Index Database
– sequence: 2
  dbid: EIF
  name: MEDLINE
  url: https://proxy.k.utb.cz/login?url=https://www.webofscience.com/wos/medline/basic-search
  sourceTypes: Index Database
DeliveryMethod fulltext_linktorsrc
Discipline Sciences (General)
Agriculture
DocumentTitleAlternate Agriculture favors resistance to biocontrol
EISSN 1091-6490
EndPage 3890
ExternalDocumentID PMC5393207
28289202
10_1073_pnas_1618416114
26480833
Genre Research Support, Non-U.S. Gov't
Journal Article
Feature
GeographicLocations New Zealand
GeographicLocations_xml – name: New Zealand
GrantInformation_xml – fundername: Agricultural and Marketing Research and Development Trust (AGMARDT)
  grantid: P15018
GroupedDBID ---
-DZ
-~X
.55
0R~
123
29P
2AX
2FS
2WC
4.4
53G
5RE
5VS
85S
AACGO
AAFWJ
AANCE
ABBHK
ABOCM
ABPLY
ABPPZ
ABTLG
ABXSQ
ABZEH
ACGOD
ACHIC
ACIWK
ACNCT
ACPRK
ADQXQ
ADULT
AENEX
AEUPB
AEXZC
AFFNX
AFOSN
AFRAH
ALMA_UNASSIGNED_HOLDINGS
AQVQM
BKOMP
CS3
D0L
DCCCD
DIK
DU5
E3Z
EBS
EJD
F5P
FRP
GX1
H13
HH5
HYE
IPSME
JAAYA
JBMMH
JENOY
JHFFW
JKQEH
JLS
JLXEF
JPM
JSG
JST
KQ8
L7B
LU7
N9A
N~3
O9-
OK1
PNE
PQQKQ
R.V
RHI
RNA
RNS
RPM
RXW
SA0
SJN
TAE
TN5
UKR
W8F
WH7
WOQ
WOW
X7M
XSW
Y6R
YBH
YKV
YSK
ZCA
~02
~KM
AAYXX
CITATION
CGR
CUY
CVF
ECM
EIF
NPM
7QG
7QL
7QP
7QR
7SN
7SS
7T5
7TK
7TM
7TO
7U9
8FD
C1K
FR3
H94
M7N
P64
RC3
7X8
5PM
ID FETCH-LOGICAL-c509t-c578e2fcb851268816601c27eb5aafd0a8115c23b5b4c7816171fa0a5d6e84003
ISSN 0027-8424
1091-6490
IngestDate Thu Aug 21 14:13:41 EDT 2025
Fri Jul 11 13:17:54 EDT 2025
Mon Jun 30 08:13:50 EDT 2025
Mon Jul 21 05:45:05 EDT 2025
Thu Apr 24 22:54:43 EDT 2025
Tue Jul 01 03:19:32 EDT 2025
Fri May 30 11:46:39 EDT 2025
IsDoiOpenAccess false
IsOpenAccess true
IsPeerReviewed true
IsScholarly true
Issue 15
Keywords meta-analysis
natural enemy
GAMM
invasive species
attack rates
Language English
LinkModel OpenURL
MergedId FETCHMERGED-LOGICAL-c509t-c578e2fcb851268816601c27eb5aafd0a8115c23b5b4c7816171fa0a5d6e84003
Notes SourceType-Scholarly Journals-1
ObjectType-Feature-1
content type line 14
ObjectType-Article-1
ObjectType-Feature-2
content type line 23
Author contributions: F.T., J.M.T., and S.L.G. designed research; F.T. performed research; F.T. and M.R. analyzed data; and F.T., J.M.T., and S.L.G. led the writing of the paper with the contribution of M.R. and S.W.
Edited by May R. Berenbaum, University of Illinois at Urbana–Champaign, Urbana, IL, and approved February 14, 2017 (received for review November 6, 2016)
ORCID 0000-0002-5168-8277
0000-0003-3747-2119
0000-0002-4831-0337
0000-0001-7402-5620
0000-0003-0057-6969
OpenAccessLink https://www.pnas.org/content/pnas/114/15/3885.full.pdf
PMID 28289202
PQID 1896938452
PQPubID 42026
PageCount 6
ParticipantIDs pubmedcentral_primary_oai_pubmedcentral_nih_gov_5393207
proquest_miscellaneous_1877527160
proquest_journals_1896938452
pubmed_primary_28289202
crossref_citationtrail_10_1073_pnas_1618416114
crossref_primary_10_1073_pnas_1618416114
jstor_primary_26480833
ProviderPackageCode CITATION
AAYXX
PublicationCentury 2000
PublicationDate 2017-04-11
PublicationDateYYYYMMDD 2017-04-11
PublicationDate_xml – month: 04
  year: 2017
  text: 2017-04-11
  day: 11
PublicationDecade 2010
PublicationPlace United States
PublicationPlace_xml – name: United States
– name: Washington
PublicationSeriesTitle From the Cover
PublicationTitle Proceedings of the National Academy of Sciences - PNAS
PublicationTitleAlternate Proc Natl Acad Sci U S A
PublicationYear 2017
Publisher National Academy of Sciences
Publisher_xml – name: National Academy of Sciences
References e_1_3_3_50_2
Box GE (e_1_3_3_56_2) 2015
e_1_3_3_16_2
e_1_3_3_18_2
e_1_3_3_39_2
e_1_3_3_12_2
Statistics New Zealand (e_1_3_3_29_2) 2012
e_1_3_3_37_2
e_1_3_3_58_2
e_1_3_3_33_2
Ives WGH (e_1_3_3_45_2) 1981
e_1_3_3_54_2
Goldson SL (e_1_3_3_35_2) 2015; 68
e_1_3_3_10_2
e_1_3_3_31_2
e_1_3_3_52_2
Topping CJ (e_1_3_3_30_2) 1997; 21
Gerard PJ (e_1_3_3_40_2) 2000
e_1_3_3_5_2
e_1_3_3_7_2
Henter HJ (e_1_3_3_44_2) 1995; 49
e_1_3_3_9_2
e_1_3_3_27_2
e_1_3_3_23_2
e_1_3_3_48_2
e_1_3_3_25_2
e_1_3_3_46_2
LCDB2 Project Development Team (e_1_3_3_63_2) 2004
e_1_3_3_1_2
e_1_3_3_3_2
e_1_3_3_21_2
e_1_3_3_42_2
e_1_3_3_51_2
Fenner F (e_1_3_3_14_2) 1999
Kabacoff R (e_1_3_3_62_2) 2011
Prestidge RA (e_1_3_3_19_2) 1991
e_1_3_3_17_2
e_1_3_3_38_2
e_1_3_3_13_2
e_1_3_3_59_2
e_1_3_3_15_2
e_1_3_3_34_2
e_1_3_3_57_2
e_1_3_3_32_2
e_1_3_3_55_2
e_1_3_3_11_2
e_1_3_3_53_2
e_1_3_3_60_2
e_1_3_3_6_2
e_1_3_3_8_2
e_1_3_3_28_2
Snyder WE (e_1_3_3_49_2) 2012
e_1_3_3_47_2
Popay AJ (e_1_3_3_24_2) 2011; 64
e_1_3_3_26_2
Barlow ND (e_1_3_3_36_2) 1993
e_1_3_3_2_2
e_1_3_3_20_2
e_1_3_3_43_2
McNeill MR (e_1_3_3_61_2) 2011; 64
e_1_3_3_4_2
e_1_3_3_22_2
e_1_3_3_41_2
28341708 - Proc Natl Acad Sci U S A. 2017 Apr 11;114(15):3792-3794
References_xml – ident: e_1_3_3_59_2
  doi: 10.1002/jae.659
– ident: e_1_3_3_41_2
  doi: 10.1126/science.291.5511.2141
– ident: e_1_3_3_57_2
  doi: 10.1093/biomet/65.2.297
– ident: e_1_3_3_18_2
  doi: 10.1086/283012
– ident: e_1_3_3_33_2
  doi: 10.1080/00288230809510453
– ident: e_1_3_3_25_2
  doi: 10.1111/j.1461-0248.2008.01250.x
– ident: e_1_3_3_58_2
  doi: 10.2307/2951597
– volume-title: R in Action: Data Analysis and Graphics with R
  year: 2011
  ident: e_1_3_3_62_2
– volume: 49
  start-page: 427
  year: 1995
  ident: e_1_3_3_44_2
  article-title: The potential for co-evolution in a host-parasitoid system. I. Genetic variation within an aphid population in susceptibility to a parasitic wasp
  publication-title: Evolution
– ident: e_1_3_3_5_2
  doi: 10.2307/1311994
– volume-title: Biological Control of Vertebrate Pests: A History of Myxomatosis—An Experiment in Coevolution
  year: 1999
  ident: e_1_3_3_14_2
  doi: 10.1079/9780851993232.0000
– ident: e_1_3_3_21_2
  doi: 10.1007/BF02373087
– ident: e_1_3_3_8_2
  doi: 10.1641/0006-3568(2006)56[311:TEVOES]2.0.CO;2
– ident: e_1_3_3_16_2
  doi: 10.2307/5485
– ident: e_1_3_3_2_2
  doi: 10.1146/annurev.en.36.010191.003021
– ident: e_1_3_3_10_2
  doi: 10.1146/annurev.en.39.010194.000403
– ident: e_1_3_3_53_2
  doi: 10.1093/ee/27.6.1386
– ident: e_1_3_3_48_2
  doi: 10.1016/j.biocontrol.2007.08.006
– ident: e_1_3_3_34_2
  doi: 10.3389/fpls.2016.01259
– ident: e_1_3_3_20_2
  doi: 10.1093/jee/99.2.273
– ident: e_1_3_3_31_2
  doi: 10.1016/0167-8809(89)90021-2
– ident: e_1_3_3_23_2
  doi: 10.1016/j.cois.2014.09.003
– ident: e_1_3_3_26_2
  doi: 10.1017/S0007485300042152
– ident: e_1_3_3_51_2
  doi: 10.1146/annurev.ento.45.1.175
– ident: e_1_3_3_52_2
  doi: 10.1080/03014223.1998.9518148
– ident: e_1_3_3_4_2
  doi: 10.1126/science.231.4743.1255
– volume-title: New Zealand Land Cover Database 2, User Guide
  year: 2004
  ident: e_1_3_3_63_2
– volume-title: Time Series Analysis: Forecasting and Control
  year: 2015
  ident: e_1_3_3_56_2
– ident: e_1_3_3_17_2
  doi: 10.1016/S0169-5347(97)87378-8
– volume: 21
  start-page: 121
  year: 1997
  ident: e_1_3_3_30_2
  article-title: Spider density and diversity in relation to disturbance in agroecosystems in New Zealand, with a comparison to England
  publication-title: N Z J Ecol
– ident: e_1_3_3_47_2
  doi: 10.1007/BF02373133
– ident: e_1_3_3_60_2
  doi: 10.1007/s004420100716
– start-page: 165
  volume-title: Proceedings of the Forty Fourth New Zealand Weed and Pest Control Conference
  year: 1991
  ident: e_1_3_3_19_2
– ident: e_1_3_3_1_2
  doi: 10.1126/science.1057544
– ident: e_1_3_3_12_2
  doi: 10.1098/rstb.1988.0001
– ident: e_1_3_3_27_2
  doi: 10.1126/science.1206360
– ident: e_1_3_3_50_2
  doi: 10.1111/j.1461-0248.2006.00922.x
– ident: e_1_3_3_28_2
  doi: 10.1007/BF01237660
– volume-title: 2012 New Zealand Census of Population and Dwellings
  year: 2012
  ident: e_1_3_3_29_2
– start-page: 23
  volume-title: Biodiversity and Insect Pests: Key Issues for Sustainable Management
  year: 2012
  ident: e_1_3_3_49_2
– volume: 68
  start-page: 204
  year: 2015
  ident: e_1_3_3_35_2
  article-title: Effect of Epichloë endophyte strains in Lolium spp. cultivars on Argentine stem weevil parasitism by Microctonus hyperodae
  publication-title: N Z Plant Prot
– ident: e_1_3_3_46_2
  doi: 10.1146/annurev.en.36.010191.002413
– ident: e_1_3_3_42_2
  doi: 10.1007/s10905-005-5614-x
– volume: 64
  start-page: 284
  year: 2011
  ident: e_1_3_3_61_2
  article-title: Weevils in pasture: A comparison of sampling techniques
  publication-title: N Z Plant Prot
– volume: 64
  start-page: 55
  year: 2011
  ident: e_1_3_3_24_2
  article-title: The current status of Argentine stem weevil (Listronotus bonariensis) as a pest in the North Island of New Zealand
  publication-title: N Z Plant Prot
– ident: e_1_3_3_22_2
  doi: 10.1016/S1049-9644(02)00018-X
– ident: e_1_3_3_39_2
  doi: 10.1016/j.cub.2014.04.053
– ident: e_1_3_3_32_2
  doi: 10.1080/03014223.2013.794847
– ident: e_1_3_3_43_2
  doi: 10.2307/5577
– ident: e_1_3_3_55_2
  doi: 10.1080/03014223.1981.10427942
– ident: e_1_3_3_11_2
  doi: 10.1890/0012-9658(1997)078[1673:WIBCES]2.0.CO;2
– ident: e_1_3_3_7_2
  doi: 10.1126/science.1185383
– ident: e_1_3_3_13_2
  doi: 10.1038/38483
– start-page: 326
  volume-title: Proceedings of the Sixth Australasian Conference on Grassland Invertebrate Ecology
  year: 1993
  ident: e_1_3_3_36_2
– ident: e_1_3_3_3_2
  doi: 10.1038/ncomms12986
– ident: e_1_3_3_15_2
  doi: 10.1038/35015069
– ident: e_1_3_3_6_2
  doi: 10.1038/nature01014
– ident: e_1_3_3_9_2
  doi: 10.1016/j.biocontrol.2014.02.012
– ident: e_1_3_3_37_2
  doi: 10.1086/282265
– ident: e_1_3_3_38_2
  doi: 10.1111/j.1752-4571.2010.00166.x
– start-page: 369
  volume-title: Biological Control Programmes Against Insects and Weeds in Canada, 1969–1980
  year: 1981
  ident: e_1_3_3_45_2
– start-page: 406
  volume-title: Proceedings of the New Zealand Plant Protection Conference
  year: 2000
  ident: e_1_3_3_40_2
– ident: e_1_3_3_54_2
  doi: 10.1080/09583159409355347
– reference: 28341708 - Proc Natl Acad Sci U S A. 2017 Apr 11;114(15):3792-3794
SSID ssj0009580
Score 2.5000737
Snippet Increased regulation of chemical pesticides and rapid evolution of pesticide resistance have increased calls for sustainable pest management. Biological...
The need for agricultural production to meet the food demands of a growing human population will require sustainable and acceptable pest management, such as...
SourceID pubmedcentral
proquest
pubmed
crossref
jstor
SourceType Open Access Repository
Aggregation Database
Index Database
Enrichment Source
Publisher
StartPage 3885
SubjectTerms Agricultural management
Agriculture
Agriculture - methods
Agrochemicals
Animals
Biodiversity
Biological control
Biological evolution
Biological Sciences
Chemical attack
Chemical pest control
Climate change
Evolution
Grasses
Host plants
Host-Parasite Interactions
Hymenoptera
Intensive farming
Introduced Species
New Zealand
Parasites
Parasitism
Parasitoids
Pasture
Pest control
Pest Control, Biological - methods
Pest resistance
Pesticide resistance
Pesticides
Pests
Predators
SEE COMMENTARY
Species diversity
Sustainable agriculture
Viability
Weevils
Title Intensified agriculture favors evolved resistance to biological control
URI https://www.jstor.org/stable/26480833
https://www.ncbi.nlm.nih.gov/pubmed/28289202
https://www.proquest.com/docview/1896938452
https://www.proquest.com/docview/1877527160
https://pubmed.ncbi.nlm.nih.gov/PMC5393207
Volume 114
hasFullText 1
inHoldings 1
isFullTextHit
isPrint
link http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV3db9MwELdgvPCCGDAIDBQkHoaqlMR2YudxQusmNMoeUtG3yHYdQEIpWrNJ8NdzFzsfHUUavFiVv1L5zuc7--53hLyJVcpUxtNIaE0jbmgeKVNlUW6qGJ-BdNJC5n-cZ2cL_mGZLkcvphhd0uip-bUzruR_qAp1QFeMkv0HyvaTQgX8BvpCCRSG8lY09v7nFaqR6sulh9Gwk0pdYw4dC6Ln2mJ4yga1RNzCoGk62CUPDNL6qY8V1Iv-QNt07gPz7r7weIg-8SJhM4kmF_Mhl3GB3ka2aVMzTWaIUwGM1jf-xCsV1Fidey7mPhxAtG3n2Aw7rx_yGTGWnWBs06-N7yjg3EMwxGQkVkEriTLuEoNO7Y66Tha7iNKO6dKRaGXS5fb5Q-aDkMJExbXaTBH9Hy02P8sWuvb8UzlbnJ-XxcmyuEvuUTArUJCfLpMRSLN06BX-n3VQUIK9uzH9lhbjHFl3mSg3PW1HqkvxkDzwNkd47Bhon9yx9SOy35EwPPLQ428fk9MRR4UjjgodR4Weo8KBo8JmHQ4cFXqOekIWs5Pi_VnkU21EBjTGBkohLa2MBgWcZhIfk-PEUGF1qlS1ipUEy8FQplPNjZBoFCeVgo2-yqyEY4AdkL16XdtnJFQcdrhZ0VjoFRdcKtA4dW6ZMSvNWWwCMu2WrjQehx7ToXwvW38IwUpc63JY64Ac9QN-OAiWv3c9aGnR90P_TTAyWEAOO-KUfgPDOJlnOZM8pQF53TeDeMU3M1Xb9RX2ESKlIsnigDx1tBwmx9sKGsNosUXlvgNCt2-31N--thDuKQO7KRbPb_HdF-T-sKUOyV5zeWVfgiLc6Fct9_4GEXO2Xw
linkProvider Geneva Foundation for Medical Education and Research
openUrl ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Intensified+agriculture+favors+evolved+resistance+to+biological+control&rft.jtitle=Proceedings+of+the+National+Academy+of+Sciences+-+PNAS&rft.au=Tomasetto%2C+Federico&rft.au=Tylianakis%2C+Jason+M&rft.au=Reale%2C+Marco&rft.au=Wratten%2C+Steve&rft.date=2017-04-11&rft.issn=1091-6490&rft.eissn=1091-6490&rft.volume=114&rft.issue=15&rft.spage=3885&rft_id=info:doi/10.1073%2Fpnas.1618416114&rft.externalDBID=NO_FULL_TEXT
thumbnail_l http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=0027-8424&client=summon
thumbnail_m http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=0027-8424&client=summon
thumbnail_s http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=0027-8424&client=summon