{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,2,21]],"date-time":"2025-02-21T13:07:22Z","timestamp":1740143242065,"version":"3.37.3"},"reference-count":47,"publisher":"Public Library of Science (PLoS)","issue":"9","license":[{"start":{"date-parts":[[2022,9,15]],"date-time":"2022-09-15T00:00:00Z","timestamp":1663200000000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100008316","name":"Baden-W\u00fcrttemberg Stiftung","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100008316","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Young Scholar Fund","award":["83943018FP430_\/18"],"award-info":[{"award-number":["83943018FP430_\/18"]}]},{"name":"AFF"},{"name":"DFG Centre of Excellence 2117 \u2018Centre for the Advanced Study of Collective Behaviour\u2019","award":["ID: 422037984"],"award-info":[{"award-number":["ID: 422037984"]}]},{"name":"DFG Centre of Excellence 2117 \u2018Centre for the Advanced Study of Collective Behaviour\u2019","award":["ID: 422037984"],"award-info":[{"award-number":["ID: 422037984"]}]},{"name":"DFG Centre of Excellence 2117 \u2018Centre for the Advanced Study of Collective Behaviour\u2019","award":["ID: 422037984"],"award-info":[{"award-number":["ID: 422037984"]}]},{"DOI":"10.13039\/501100001824","name":"Grantov\u00e1 Agentura \u010cesk\u00e9 Republiky","doi-asserted-by":"publisher","award":["GA22-10845S"],"award-info":[{"award-number":["GA22-10845S"]}],"id":[{"id":"10.13039\/501100001824","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100010583","name":"Universit\u00e4t Konstanz","doi-asserted-by":"publisher","award":["Zukunftskolleg"],"award-info":[{"award-number":["Zukunftskolleg"]}],"id":[{"id":"10.13039\/501100010583","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001659","name":"Deutsche Forschungsgemeinschaft","doi-asserted-by":"crossref","award":["414260764"],"award-info":[{"award-number":["414260764"]}],"id":[{"id":"10.13039\/501100001659","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":["www.ploscompbiol.org"],"crossmark-restriction":false},"short-container-title":["PLoS Comput Biol"],"abstract":"<jats:p>Honeybees protect their colony against vertebrates by mass stinging and they coordinate their actions during this crucial event thanks to an alarm pheromone carried directly on the stinger, which is therefore released upon stinging. The pheromone then recruits nearby bees so that more and more bees participate in the defence. However, a quantitative understanding of how an individual bee adapts its stinging response during the course of an attack is still a challenge: Typically, only the group behaviour is effectively measurable in experiment; Further, linking the observed group behaviour with individual responses requires a probabilistic model enumerating a combinatorial number of possible group contexts during the defence; Finally, extracting the individual characteristics from group observations requires novel methods for parameter inference.<\/jats:p><jats:p>We first experimentally observed the behaviour of groups of bees confronted with a fake predator inside an arena and quantified their defensive reaction by counting the number of stingers embedded in the dummy at the end of a trial. We propose a biologically plausible model of this phenomenon, which transparently links the choice of each individual bee to sting or not, to its group context at the time of the decision. Then, we propose an efficient method for inferring the parameters of the model from the experimental data. Finally, we use this methodology to investigate the effect of group size on stinging initiation and alarm pheromone recruitment.<\/jats:p><jats:p>Our findings shed light on how the social context influences stinging behaviour, by quantifying how the alarm pheromone concentration level affects the decision of each bee to sting or not in a given group size. We show that recruitment is curbed as group size grows, thus suggesting that the presence of nestmates is integrated as a negative cue by individual bees. Moreover, the unique integration of exact and statistical methods provides a quantitative characterisation of uncertainty associated to each of the inferred parameters.<\/jats:p>","DOI":"10.1371\/journal.pcbi.1010305","type":"journal-article","created":{"date-parts":[[2022,9,15]],"date-time":"2022-09-15T17:26:10Z","timestamp":1663262770000},"page":"e1010305","update-policy":"https:\/\/doi.org\/10.1371\/journal.pcbi.corrections_policy","source":"Crossref","is-referenced-by-count":7,"title":["Extracting individual characteristics from population data reveals a negative social effect during honeybee defence"],"prefix":"10.1371","volume":"18","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-9041-0905","authenticated-orcid":true,"given":"Tatjana","family":"Petrov","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Matej","family":"Hajnal","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8972-159X","authenticated-orcid":true,"given":"Julia","family":"Klein","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0713-2431","authenticated-orcid":true,"given":"David","family":"\u0160afr\u00e1nek","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Morgane","family":"Nouvian","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"340","published-online":{"date-parts":[[2022,9,15]]},"reference":[{"issue":"4","key":"pcbi.1010305.ref001","doi-asserted-by":"crossref","first-page":"521","DOI":"10.1098\/rsbl.2011.0067","article-title":"Synergy between social and private information increases foraging efficiency in ants","volume":"7","author":"TJ Czaczkes","year":"2011","journal-title":"Biology Letters"},{"issue":"1564","key":"pcbi.1010305.ref002","first-page":"705","article-title":"Amplification of individual preferences in a social context: the case of wall-following in ants","volume":"272","author":"A Dussutour","year":"2005","journal-title":"Proceedings of the Royal Society of London, Series B: Biological Sciences"},{"issue":"6119","key":"pcbi.1010305.ref003","doi-asserted-by":"crossref","first-page":"574","DOI":"10.1126\/science.1225883","article-title":"Emergent sensing of complex environments by mobile animal groups","volume":"339","author":"A Berdahl","year":"2013","journal-title":"Science"},{"key":"pcbi.1010305.ref004","doi-asserted-by":"crossref","first-page":"297","DOI":"10.1016\/j.anbehav.2015.10.032","article-title":"Social context modulates idiosyncrasy of behaviour in the gregarious cockroach Blaberus discoidalis","volume":"111","author":"JD Crall","year":"2016","journal-title":"Animal Behaviour"},{"issue":"1","key":"pcbi.1010305.ref005","doi-asserted-by":"crossref","first-page":"15836","DOI":"10.1038\/s41598-018-33917-7","article-title":"Behavioral flexibility promotes collective consistency in a social insect","volume":"8","author":"LK Garrison","year":"2018","journal-title":"Sci Rep"},{"issue":"9","key":"pcbi.1010305.ref006","doi-asserted-by":"crossref","first-page":"e0183872","DOI":"10.1371\/journal.pone.0183872","article-title":"Social interactions promote adaptive resource defense in ants","volume":"12","author":"CJ Kleineidam","year":"2017","journal-title":"PLoS One"},{"issue":"2","key":"pcbi.1010305.ref007","doi-asserted-by":"crossref","first-page":"323","DOI":"10.1016\/j.anbehav.2013.05.021","article-title":"Social context influences the initiation and threshold of thermoregulatory behaviour in honeybees","volume":"86","author":"CN Cook","year":"2013","journal-title":"Animal Behaviour"},{"issue":"7","key":"pcbi.1010305.ref008","doi-asserted-by":"crossref","first-page":"170232","DOI":"10.1098\/rsos.170232","article-title":"Group choices seemingly at odds with individual preferences","volume":"4","author":"MO Laurent Salazar","year":"2017","journal-title":"Royal Society Open Science"},{"issue":"1","key":"pcbi.1010305.ref009","doi-asserted-by":"crossref","first-page":"20331","DOI":"10.1038\/s41598-019-56504-w","article-title":"Conflictual influence of humidity during shelter selection of the American cockroach (Periplaneta americana)","volume":"9","author":"M Calvo Martin","year":"2019","journal-title":"Scientific Reports"},{"issue":"22","key":"pcbi.1010305.ref010","doi-asserted-by":"crossref","first-page":"3505","DOI":"10.1242\/jeb.143016","article-title":"The defensive response of the honeybee Apis mellifera","volume":"219","author":"M Nouvian","year":"2016","journal-title":"J Exp Biol"},{"issue":"6","key":"pcbi.1010305.ref011","doi-asserted-by":"crossref","first-page":"539","DOI":"10.1007\/s00265-003-0662-8","article-title":"Effects of colony size and stage of development on defense response by the swarm-founding wasp Polybia occidentalis","volume":"54","author":"KB London","year":"2003","journal-title":"Behavioral Ecology and Sociobiology"},{"key":"pcbi.1010305.ref012","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1111\/j.1439-0310.1987.tb00668.x","article-title":"Group response to alarm pheromones in social wasp and the honeybee","volume":"76","author":"RFA Moritz","year":"1987","journal-title":"Ethology"},{"key":"pcbi.1010305.ref013","first-page":"1","article-title":"Effect of group size on the aggression strategy of an extirpating stingless bee, Trigona spinipes","volume":"52","author":"JC Nieh","year":"2005","journal-title":"Insectes Sociaux"},{"issue":"1","key":"pcbi.1010305.ref014","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/ncomms10247","article-title":"Appetitive floral odours prevent aggression in honeybees","volume":"6","author":"M Nouvian","year":"2015","journal-title":"Nature communications"},{"key":"pcbi.1010305.ref015","doi-asserted-by":"crossref","first-page":"214","DOI":"10.1007\/978-3-319-21690-4_13","volume-title":"Computer Aided Verification","author":"C Dehnert","year":"2015"},{"key":"pcbi.1010305.ref016","doi-asserted-by":"crossref","first-page":"660","DOI":"10.1007\/978-3-642-14295-6_56","volume-title":"Computer Aided Verification","author":"EM Hahn","year":"2010"},{"key":"pcbi.1010305.ref017","article-title":"Parameter Synthesis for Markov Models","author":"S Junges","year":"2019","journal-title":"CoRR"},{"key":"pcbi.1010305.ref018","doi-asserted-by":"crossref","unstructured":"Katoen JP. The probabilistic model checking landscape. In: Proceedings of the 31st Annual ACM\/IEEE Symposium on Logic in Computer Science. ACM; 2016. p. 31\u201345.","DOI":"10.1145\/2933575.2934574"},{"key":"pcbi.1010305.ref019","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1007\/978-3-319-43425-4_3","volume-title":"Quantitative Evaluation of Systems","author":"E Polgreen","year":"2016"},{"key":"pcbi.1010305.ref020","doi-asserted-by":"crossref","first-page":"3569","DOI":"10.1016\/S1573-4412(01)05010-3","article-title":"Markov chain Monte Carlo methods: computation and inference","volume":"5","author":"S Chib","year":"2001","journal-title":"Handbook of econometrics"},{"issue":"1","key":"pcbi.1010305.ref021","doi-asserted-by":"crossref","first-page":"106","DOI":"10.1186\/s12915-021-01028-x","article-title":"Honeybee communication during collective defence is shaped by predation","volume":"19","author":"A Lopez-Incera","year":"2021","journal-title":"BMC Biology"},{"issue":"3","key":"pcbi.1010305.ref022","doi-asserted-by":"crossref","first-page":"e0193049","DOI":"10.1371\/journal.pone.0193049","article-title":"Probabilistic models of individual and collective animal behavior","volume":"13","author":"K Bod\u2019ov\u00e1","year":"2018","journal-title":"PloS one"},{"key":"pcbi.1010305.ref023","doi-asserted-by":"crossref","first-page":"592","DOI":"10.1007\/978-3-319-63390-9_31","volume-title":"Computer Aided Verification","author":"C Dehnert","year":"2017"},{"key":"pcbi.1010305.ref024","doi-asserted-by":"crossref","unstructured":"de Moura LM, Bj\u00f8rner N. Z3: An Efficient SMT Solver. In: TACAS\u201908. vol. 4963 of LNCS. Springer; 2008. p. 337\u2013340.","DOI":"10.1007\/978-3-540-78800-3_24"},{"key":"pcbi.1010305.ref025","doi-asserted-by":"crossref","unstructured":"Gao S, Kong S, Clarke EM. dReal: An SMT Solver for Nonlinear Theories over the Reals. In: CADE-24. vol. 7898 of LNCS. Springer; 2013. p. 208\u2013214.","DOI":"10.1007\/978-3-642-38574-2_14"},{"key":"pcbi.1010305.ref026","doi-asserted-by":"crossref","unstructured":"Taschini S. Interval arithmetic: python implementation and applications. In: Proc 7th Python Sci Conf (ScyPy 2008); 2008.","DOI":"10.25080\/XJFF2622"},{"issue":"9","key":"pcbi.1010305.ref027","doi-asserted-by":"crossref","first-page":"093001","DOI":"10.1088\/1751-8121\/aa54d9","article-title":"Approximation and inference methods for stochastic biochemical kinetics\u2014a tutorial review","volume":"50","author":"D Schnoerr","year":"2017","journal-title":"Journal of Physics A: Mathematical and Theoretical"},{"issue":"5","key":"pcbi.1010305.ref028","doi-asserted-by":"crossref","first-page":"512","DOI":"10.1007\/BF01211866","article-title":"A logic for reasoning about time and reliability","volume":"6","author":"H Hansson","year":"1994","journal-title":"Formal Aspects of Computing"},{"key":"pcbi.1010305.ref029","doi-asserted-by":"crossref","unstructured":"Kwiatkowska M, Norman G, Parker D. PRISM 4.0: Verification of probabilistic real-time systems. In: International conference on computer aided verification. Springer; 2011. p. 585\u2013591.","DOI":"10.1007\/978-3-642-22110-1_47"},{"issue":"6","key":"pcbi.1010305.ref030","doi-asserted-by":"crossref","first-page":"1087","DOI":"10.1063\/1.1699114","article-title":"Equation of state calculations by fast computing machines","volume":"21","author":"N Metropolis","year":"1953","journal-title":"The journal of chemical physics"},{"key":"pcbi.1010305.ref031","article-title":"Interspecific social networks promote information transmission in wild songbirds","volume":"282","author":"DR Farine","year":"2015","journal-title":"Proceedings of the Royal Society B: Biological Sciences"},{"key":"pcbi.1010305.ref032","unstructured":"Akaike H. Information theory and an extension of the maximum likelihood principle. In: Second International Symposium on Information Theory. B.N. Petrov and B.F. Csaki (Eds.). Academiai Kiado: Budapest; 1973. p. 267\u2013281."},{"issue":"5","key":"pcbi.1010305.ref033","doi-asserted-by":"crossref","first-page":"399","DOI":"10.1016\/j.jinsphys.2007.01.010","article-title":"Flight and fight: a comparative view of the neurophysiology and genetics of honey bee defensive behavior","volume":"53","author":"GJ Hunt","year":"2007","journal-title":"J Insect Physiol"},{"issue":"5","key":"pcbi.1010305.ref034","doi-asserted-by":"crossref","first-page":"613","DOI":"10.1007\/BF00611934","article-title":"Modulation of alarm pheromone perception in the honey bee: evidence for division of labor based on hormonally regulated response thresholds","volume":"160","author":"GE Robinson","year":"1987","journal-title":"Journal of Comparative Physiology, A"},{"key":"pcbi.1010305.ref035","doi-asserted-by":"crossref","first-page":"637","DOI":"10.1146\/annurev.en.37.010192.003225","article-title":"Regulation of division of labor in insect societies","volume":"37","author":"GE Robinson","year":"1992","journal-title":"Annual Review of Entomology"},{"key":"pcbi.1010305.ref036","doi-asserted-by":"crossref","first-page":"1018","DOI":"10.1038\/1951018b0","article-title":"Identification of isoamyl acetate as an active component in the sting pheromone of the honey bee","volume":"195","author":"R Boch","year":"1962","journal-title":"Nature"},{"issue":"11","key":"pcbi.1010305.ref037","doi-asserted-by":"crossref","first-page":"e0185325","DOI":"10.1371\/journal.pone.0185325","article-title":"\u201cUp\u201d or \u201cdown\u201d that makes the difference. How giant honeybees (Apis dorsata) see the world","volume":"12","author":"N Koeniger","year":"2017","journal-title":"PLoS One"},{"issue":"1871","key":"pcbi.1010305.ref038","article-title":"Cooperative defence operates by social modulation of biogenic amine levels in the honey bee brain","volume":"285","author":"M Nouvian","year":"2018","journal-title":"Proceedings of the Royal Society of London, Series B: Biological Sciences"},{"issue":"1","key":"pcbi.1010305.ref039","doi-asserted-by":"crossref","first-page":"65","DOI":"10.1007\/s10905-008-9155-y","article-title":"Aggressive and Docile Colony Defence Patterns in Apis mellifera. A Retreater\u2013Releaser Concept","volume":"22","author":"G Kastberger","year":"2009","journal-title":"Journal of Insect Behavior"},{"key":"pcbi.1010305.ref040","doi-asserted-by":"crossref","first-page":"1329","DOI":"10.1603\/0013-8746(2000)093[1329:DHBSAP]2.0.CO;2","article-title":"Does Honey Bee sting alarm pheromone give orientation information to defensive bees?","volume":"93","author":"BR Wager","year":"2000","journal-title":"Ann Entomol Soc Am"},{"key":"pcbi.1010305.ref041","doi-asserted-by":"crossref","first-page":"193","DOI":"10.1016\/0003-3472(61)90008-2","article-title":"The stimuli releasing the stinging response of honeybees","volume":"9","author":"JB Free","year":"1961","journal-title":"Anim Behav"},{"key":"pcbi.1010305.ref042","doi-asserted-by":"crossref","first-page":"16","DOI":"10.1186\/s12983-017-0199-8","article-title":"Sequential social experiences interact to modulate aggression but not brain gene expression in the honey bee (Apis mellifera)","volume":"14","author":"CC Rittschof","year":"2017","journal-title":"Front Zool"},{"key":"pcbi.1010305.ref043","doi-asserted-by":"crossref","first-page":"262","DOI":"10.1163\/156853951X00179","article-title":"The Behaviour of Worker Honeybees At the Hive Entrance","volume":"4","author":"CG Butler","year":"1952","journal-title":"Behaviour"},{"issue":"12","key":"pcbi.1010305.ref044","doi-asserted-by":"crossref","first-page":"1306","DOI":"10.1007\/s10886-010-9881-4","article-title":"Alarm pheromones do not mediate rapid shifts in honey bee guard acceptance threshold","volume":"36","author":"MJ Couvillon","year":"2010","journal-title":"J Chem Ecol"},{"issue":"46","key":"pcbi.1010305.ref045","doi-asserted-by":"crossref","first-page":"18720","DOI":"10.1073\/pnas.1107583108","article-title":"Inferring the structure and dynamics of interactions in schooling fish","volume":"108","author":"Y Katz","year":"2011","journal-title":"Proceedings of the National Academy of Sciences"},{"issue":"28","key":"pcbi.1010305.ref046","doi-asserted-by":"crossref","first-page":"12576","DOI":"10.1073\/pnas.1001763107","article-title":"Inferring individual rules from collective behavior","volume":"107","author":"R Lukeman","year":"2010","journal-title":"Proceedings of the National Academy of Sciences"},{"issue":"1","key":"pcbi.1010305.ref047","doi-asserted-by":"crossref","DOI":"10.1016\/0890-5401(90)90004-2","article-title":"Symmetry Breaking in Distributed Networks","volume":"88","author":"A Itai","year":"1990","journal-title":"Information and Computation"}],"container-title":["PLOS Computational Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pcbi.1010305","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,10,3]],"date-time":"2024-10-03T23:03:56Z","timestamp":1727996636000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pcbi.1010305"}},"subtitle":[],"editor":[{"given":"Ricardo","family":"Martinez-Garcia","sequence":"first","affiliation":[],"role":[{"role":"editor","vocabulary":"crossref"}]}],"short-title":[],"issued":{"date-parts":[[2022,9,15]]},"references-count":47,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2022,9,15]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pcbi.1010305","relation":{},"ISSN":["1553-7358"],"issn-type":[{"type":"electronic","value":"1553-7358"}],"subject":[],"published":{"date-parts":[[2022,9,15]]}}}