{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,1]],"date-time":"2026-06-01T17:10:31Z","timestamp":1780333831927,"version":"3.54.1"},"reference-count":62,"publisher":"Wiley","issue":"16","license":[{"start":{"date-parts":[[2018,7,13]],"date-time":"2018-07-13T00:00:00Z","timestamp":1531440000000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Steven and Alexandra Cohen Foundation"}],"content-domain":{"domain":["onlinelibrary.wiley.com"],"crossmark-restriction":true},"short-container-title":["Ecology and Evolution"],"published-print":{"date-parts":[[2018,8]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:p>The blacklegged tick <jats:italic>Ixodes scapularis<\/jats:italic> is the primary vector for the bacterium causing Lyme disease in eastern North America and for other medically important pathogens. This species is vulnerable to attack by fungal pathogens and arthropod predators, but the impacts of interactions between biocontrol agents have not been examined. The biocontrol agent Met52<jats:sup>\u00ae<\/jats:sup>, containing the entomopathogenic fungus <jats:italic>Metarhizium brunneum<\/jats:italic> (=<jats:italic>M.\u00a0anisopliae<\/jats:italic>), controls blacklegged ticks with efficacy comparable to chemical acaricides. The brush\u2010legged wolf spider <jats:italic>Schizocosa ocreata<\/jats:italic> is a predator of <jats:italic>I.\u00a0scapularis<\/jats:italic> that reduces their survival under field conditions. We conducted a field microcosm experiment to assess the compatibility of Met52 and <jats:italic>S.\u00a0ocreata<\/jats:italic> as tick biocontrol agents. We compared the fits of alternative models in predicting survival of unfed (flat) and blood\u2010fed (engorged) nymphs. We found the strongest support for a model that included negative effects of Met52 and <jats:italic>S.\u00a0ocreata<\/jats:italic> on flat nymph survival. We found evidence for interference between biocontrol agents, with Met52 reducing spider survival, but we did not find a significant interaction effect between the two agents on nymph survival. For engorged nymphs, low recovery rates resulted in low statistical power to detect possible effects of biocontrol agents. We found that nymph questing activity was lower when the spider was active above the leaf litter than when the spider was unobserved. This provides the first evidence that predation cues might affect behavior important for tick fitness and pathogen transmission. This study presents field microcosm evidence that the biopesticide Met52 and spider <jats:italic>Schizocosa ocreata<\/jats:italic> each reduced survival of blacklegged ticks <jats:italic>Ixodes scapularis<\/jats:italic>. Met52 reduced spider survival. Potential interference between Met52 and the spider should be examined at larger scales, where overlap patterns may differ. Ticks were more likely to quest when the spider was inactive, suggesting the ticks changed their behavior to reduce danger.<\/jats:p>","DOI":"10.1002\/ece3.4271","type":"journal-article","created":{"date-parts":[[2018,7,13]],"date-time":"2018-07-13T12:20:37Z","timestamp":1531484437000},"page":"7824-7834","update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":15,"title":["Tritrophic interactions between a fungal pathogen, a spider predator, and the blacklegged tick"],"prefix":"10.1002","volume":"8","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-6956-8284","authenticated-orcid":false,"given":"Ilya R.","family":"Fischhoff","sequence":"first","affiliation":[{"name":"Cary Institute of Ecosystem Studies  Millbrook New York"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"James C.","family":"Burtis","sequence":"additional","affiliation":[{"name":"Department of Natural Resources Cornell University  Ithaca New York"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Felicia","family":"Keesing","sequence":"additional","affiliation":[{"name":"Bard College  Annandale\u2010on\u2010Hudson New York"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3707-9301","authenticated-orcid":false,"given":"Richard S.","family":"Ostfeld","sequence":"additional","affiliation":[{"name":"Cary Institute of Ecosystem Studies  Millbrook New York"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"311","published-online":{"date-parts":[[2018,7,13]]},"reference":[{"key":"e_1_2_10_2_1","doi-asserted-by":"publisher","DOI":"10.1186\/s12889-015-2629-x"},{"key":"e_1_2_10_3_1","doi-asserted-by":"publisher","DOI":"10.1023\/A:1013554517148"},{"key":"e_1_2_10_4_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.vetpar.2007.03.030"},{"key":"e_1_2_10_5_1","doi-asserted-by":"publisher","DOI":"10.2307\/3803155"},{"key":"e_1_2_10_6_1","doi-asserted-by":"publisher","DOI":"10.1093\/jmedent\/47.5.862"},{"key":"e_1_2_10_7_1","doi-asserted-by":"publisher","DOI":"10.3852\/07-202"},{"key":"e_1_2_10_8_1","doi-asserted-by":"publisher","DOI":"10.1890\/06-1707.1"},{"key":"e_1_2_10_9_1","doi-asserted-by":"publisher","DOI":"10.1525\/california\/9780520274884.001.0001"},{"key":"e_1_2_10_10_1","doi-asserted-by":"publisher","DOI":"10.1603\/ME12060"},{"key":"e_1_2_10_11_1","doi-asserted-by":"publisher","DOI":"10.1007\/s10905-014-9449-1"},{"key":"e_1_2_10_12_1","doi-asserted-by":"publisher","DOI":"10.1111\/een.12131"},{"key":"e_1_2_10_13_1","doi-asserted-by":"publisher","DOI":"10.1007\/s00442-015-3226-5"},{"key":"e_1_2_10_14_1","doi-asserted-by":"publisher","DOI":"10.1093\/jme\/tjx157"},{"issue":"2015","key":"e_1_2_10_15_1","first-page":"225","article-title":"The relationship between soil arthropods and the overwinter survival of Ixodes scapularis (Acari: Ixodidae) under manipulated snow cover","volume":"53","author":"Burtis J. C.","year":"2015","journal-title":"Journal of Medical Entomology"},{"key":"e_1_2_10_16_1","doi-asserted-by":"publisher","DOI":"10.1002\/ecs2.1914"},{"key":"e_1_2_10_17_1","doi-asserted-by":"publisher","DOI":"10.3376\/1081-1710(2008)33[166:COASPB]2.0.CO;2"},{"key":"e_1_2_10_18_1","doi-asserted-by":"publisher","DOI":"10.1093\/jmedent\/32.2.119"},{"key":"e_1_2_10_19_1","unstructured":"European Commission. (2008).Initial risk assessment provided by the rapporteur Member State The Netherlands for the existing active substance Metarhizium anisopliae var. \u2018BIPESCO 5\/F52\u2019 (Vol. 3). Retrieved fromhttps:\/\/www.efsa.europa.eu\/en\/efsajournal\/pub\/2498"},{"key":"e_1_2_10_20_1","unstructured":"European Commission. (2014).European Commission Final Review report for the active substance Metarhizium anisopliae var. anisopliae BIPESCO 5\/F52. doi:\/10.2903\/j.efsa.2012.2498"},{"key":"e_1_2_10_21_1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0187675"},{"key":"e_1_2_10_22_1","unstructured":"Fischhoff I. R. Burtis J. C. Keesing F. &Ostfeld R. S.(2017).Dataset: Tritrophic interactions between a fungal pathogen a spider predator and the blacklegged tick. Retrieved fromhttps:\/\/figshare.com\/s\/dbe9cdc6a919f276dda7"},{"key":"e_1_2_10_23_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.ijmm.2007.10.003"},{"issue":"1","key":"e_1_2_10_24_1","first-page":"91","article-title":"Effectiveness of Metarhizium anisopliae (Deuteromycetes) against Ixodes scapularis (Acari: Ixodidae) engorging on Peromyscus leucopus","volume":"30","author":"Hornbostel V. L.","year":"2005","journal-title":"Journal of Vector Ecology"},{"key":"e_1_2_10_25_1","doi-asserted-by":"publisher","DOI":"10.1603\/0022-2585-41.5.922"},{"key":"e_1_2_10_26_1","doi-asserted-by":"publisher","DOI":"10.1007\/s00442-002-1091-5"},{"key":"e_1_2_10_27_1","unstructured":"Mazerolle M. J.(2017).AICcmodavg: Model selection and multimodel inference based on (Q)AIC(c)."},{"key":"e_1_2_10_28_1","doi-asserted-by":"publisher","DOI":"10.1111\/jzo.12127"},{"key":"e_1_2_10_29_1","first-page":"39","article-title":"Principles from community and metapopulation ecology: Application to fungal entomopathogens","volume":"55","author":"Meyling N. V.","year":"2010","journal-title":"The Ecology of Fungal Entomopathogens"},{"key":"e_1_2_10_30_1","doi-asserted-by":"publisher","DOI":"10.3201\/eid2109.150417"},{"key":"e_1_2_10_31_1","unstructured":"Novozymes Biologicals Inc. (2012).Met 52\u00aeEC (NY Product No. 70127\u201010). Retrieved fromhttp:\/\/www.dec.ny.gov\/nyspad\/products?1"},{"key":"e_1_2_10_32_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.cropro.2008.03.007"},{"key":"e_1_2_10_33_1","doi-asserted-by":"publisher","DOI":"10.1146\/annurev.es.20.110189.001501"},{"key":"e_1_2_10_34_1","doi-asserted-by":"publisher","DOI":"10.1080\/09583157.2010.517603"},{"key":"e_1_2_10_35_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.biocontrol.2004.07.005"},{"key":"e_1_2_10_36_1","doi-asserted-by":"publisher","DOI":"10.1890\/07-0260.1"},{"key":"e_1_2_10_37_1","volume-title":"R: A language and environment for statistical computing","author":"R Core Team","year":"2017"},{"key":"e_1_2_10_38_1","doi-asserted-by":"publisher","DOI":"10.1017\/S0031182004004925"},{"key":"e_1_2_10_39_1","doi-asserted-by":"publisher","DOI":"10.1111\/eea.12390"},{"key":"e_1_2_10_40_1","doi-asserted-by":"publisher","DOI":"10.1006\/bcon.1995.1038"},{"key":"e_1_2_10_41_1","doi-asserted-by":"publisher","DOI":"10.1098\/rspb.2015.2430"},{"key":"e_1_2_10_42_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.biocontrol.2015.10.003"},{"key":"e_1_2_10_43_1","doi-asserted-by":"publisher","DOI":"10.1603\/0022-2585-38.1.1"},{"key":"e_1_2_10_44_1","doi-asserted-by":"publisher","DOI":"10.1645\/0022-3395(2001)087[1355:POEFTD]2.0.CO;2"},{"key":"e_1_2_10_45_1","doi-asserted-by":"publisher","DOI":"10.1890\/0012-9658(1997)078[1388:BMTCEO]2.0.CO;2"},{"key":"e_1_2_10_46_1","doi-asserted-by":"publisher","DOI":"10.1002\/ecy.1916"},{"key":"e_1_2_10_47_1","doi-asserted-by":"publisher","DOI":"10.1603\/0022-2585-38.2.318"},{"issue":"1991","key":"e_1_2_10_48_1","first-page":"115","article-title":"The guild concept and the structure of ecological communities","volume":"22","author":"Simberloff D.","year":"2008","journal-title":"Annual Review of Ecology and Systematics"},{"key":"e_1_2_10_49_1","doi-asserted-by":"publisher","DOI":"10.1890\/13-2347.1"},{"key":"e_1_2_10_50_1","doi-asserted-by":"publisher","DOI":"10.1006\/bcon.1999.0723"},{"key":"e_1_2_10_51_1","doi-asserted-by":"publisher","DOI":"10.1603\/ME10019"},{"key":"e_1_2_10_52_1","doi-asserted-by":"publisher","DOI":"10.1603\/0022-2585-40.5.642"},{"key":"e_1_2_10_53_1","doi-asserted-by":"publisher","DOI":"10.1890\/09-0787.1"},{"key":"e_1_2_10_54_1","doi-asserted-by":"publisher","DOI":"10.1139\/Z08-114"},{"key":"e_1_2_10_55_1","unstructured":"Thang. M. H. &Shepard. B. M.(1988).Effect of Metarrhizium anisopliae and Beauveria bassiana (Deuteromycotina) and buprofezin on the brown planthopper Nilaparvata lugens (Stal) (Homoptera:Delphacidae) and the wolf spider Lycosa pseudoannulata Boes et Strand (Araneae: Lycosidae)."},{"key":"e_1_2_10_56_1","volume-title":"Spiders of North America identification manual","author":"Ubick D. P.","year":"2005"},{"key":"e_1_2_10_57_1","unstructured":"U.S. Environmental Protection Agency. (2000).Biopesticides Registration Action Document: Metarhizium anisopliae strain F52. Biopesticides Registration Action Document: Metarhizium Anisopliae Strain F52. Retrieved fromhttp:\/\/www.epa.gov\/opp00001\/methods\/atmpmethods\/QC-23-01.pdf"},{"key":"e_1_2_10_58_1","doi-asserted-by":"publisher","DOI":"10.1093\/ee\/23.2.502"},{"key":"e_1_2_10_59_1","doi-asserted-by":"publisher","DOI":"10.1560\/IJEE.56.3-4.263"},{"key":"e_1_2_10_60_1","doi-asserted-by":"publisher","DOI":"10.3758\/BF03206482"},{"key":"e_1_2_10_61_1","doi-asserted-by":"publisher","DOI":"10.2307\/2265637"},{"key":"e_1_2_10_62_1","doi-asserted-by":"publisher","DOI":"10.1139\/z02-037"},{"key":"e_1_2_10_63_1","doi-asserted-by":"publisher","DOI":"10.1093\/jmedent\/36.6.900"}],"container-title":["Ecology and Evolution"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.wiley.com\/onlinelibrary\/tdm\/v1\/articles\/10.1002%2Fece3.4271","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1002\/ece3.4271","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/full-xml\/10.1002\/ece3.4271","content-type":"application\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1002\/ece3.4271","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,9,9]],"date-time":"2023-09-09T03:07:57Z","timestamp":1694228877000},"score":1,"resource":{"primary":{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/10.1002\/ece3.4271"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2018,7,13]]},"references-count":62,"journal-issue":{"issue":"16","published-print":{"date-parts":[[2018,8]]}},"alternative-id":["10.1002\/ece3.4271"],"URL":"https:\/\/doi.org\/10.1002\/ece3.4271","archive":["Portico"],"relation":{},"ISSN":["2045-7758","2045-7758"],"issn-type":[{"value":"2045-7758","type":"print"},{"value":"2045-7758","type":"electronic"}],"subject":[],"published":{"date-parts":[[2018,7,13]]},"assertion":[{"value":"2018-01-25","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2018-05-21","order":1,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2018-07-13","order":2,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}]}}