{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,30]],"date-time":"2026-09-30T20:00:17Z","timestamp":1790798417329,"version":"4.1.0"},"reference-count":46,"publisher":"MDPI AG","issue":"8","license":[{"start":{"date-parts":[[2020,8,13]],"date-time":"2020-08-13T00:00:00Z","timestamp":1597276800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100004757","name":"General Mills","doi-asserted-by":"publisher","award":["Foundation"],"award-info":[{"award-number":["Foundation"]}],"id":[{"id":"10.13039\/100004757","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Insects"],"abstract":"<jats:p>Honey bees use several strategies to protect themselves and the colony from parasites and pathogens. In addition to individual immunity, social immunity involves the cumulative effort of some individuals to limit the spread of parasites and pathogens to uninfected nestmates. Examples of social immunity in honey bees that have received attention include hygienic behavior, or the removal of diseased brood, and the collection and deposition of antimicrobial resins (propolis) on interior nest surfaces. Advances in our understanding of another form of social immunity, social fever, are lacking. Honey bees were shown to raise the temperature of the nest in response to temperature-sensitive brood pathogen, Ascosphaera apis. The increase in nest temperature (\u22120.6 \u00b0C) is thought to limit the spread of A. apis infection to uninfected immatures. We established observation hives and monitored the temperature of the brood nest for 40 days. This observation period was broken into five distinct segments, corresponding to sucrose solution feedings\u2014Pre-Feed, Feed I, Challenge, Feed II, and Post-Feed. Ascosphaera apis was administered to colonies as a 1% solution of ground sporulating chalkbrood mummies in 50% v\/v sucrose solution, during the Challenge period. Like previous reports, we observed a modest increase in brood nest temperature during the Challenge period. However, all hives presented signs of chalkbrood disease, suggesting that elevation of the nest temperature was not sufficient to stop the spread of infection among immatures. We also began to explore the molecular mechanisms of temperature increase by exposing adult bees in cages to A. apis, without the presence of immatures. Compared to adult workers who were given sucrose solution only, workers exposed to A. apis showed increased expression of the antimicrobial peptides abaecin (p = 0.07) and hymenoptaecin (p = 0.04), but expression of the heat shock response protein Hsp 70Ab-like (p = 0.76) and the nutritional marker vitellogenin (p = 0.72) were unaffected. These results indicate that adult honey bee workers exposed to a brood pathogen elevate the temperature of the brood nest and initiate an immune response, but the effect of this fever on preventing disease requires further study.<\/jats:p>","DOI":"10.3390\/insects11080528","type":"journal-article","created":{"date-parts":[[2020,8,13]],"date-time":"2020-08-13T09:23:44Z","timestamp":1597310624000},"page":"528","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":17,"title":["Social Fever or General Immune Response? Revisiting an Example of Social Immunity in Honey Bees"],"prefix":"10.3390","volume":"11","author":[{"given":"Michael","family":"Goblirsch","sequence":"first","affiliation":[{"name":"Department of Entomology, Bee Research Facility, University of Minnesota, 1980 Folwell Avenue, St. Paul, MN 55108, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jenny F.","family":"Warner","sequence":"additional","affiliation":[{"name":"Department of Entomology, Bee Research Facility, University of Minnesota, 1980 Folwell Avenue, St. Paul, MN 55108, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Brooke A.","family":"Sommerfeldt","sequence":"additional","affiliation":[{"name":"Department of Entomology, Bee Research Facility, University of Minnesota, 1980 Folwell Avenue, St. Paul, MN 55108, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6822-3636","authenticated-orcid":false,"given":"Marla","family":"Spivak","sequence":"additional","affiliation":[{"name":"Department of Entomology, Bee Research Facility, University of Minnesota, 1980 Folwell Avenue, St. Paul, MN 55108, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2020,8,13]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"1327","DOI":"10.1126\/science.133.3461.1327","article-title":"Nest climate regulation in honey bee colonies","volume":"133","author":"Simpson","year":"1961","journal-title":"Science"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"299","DOI":"10.1007\/s00114-002-0338-7","article-title":"Hot spots in the bee hive","volume":"89","author":"Bujok","year":"2002","journal-title":"Naturwissenschaften"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"4217","DOI":"10.1242\/jeb.00680","article-title":"Hot bees in empty broodnest cells: Heating from within","volume":"206","author":"Kleinhenz","year":"2003","journal-title":"J. Exp. Biol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"e8967","DOI":"10.1371\/journal.pone.0008967","article-title":"Honeybee colony thermoregulation\u2013regulatory mechanisms and contribution of individuals in dependence on age, location and thermal stress","volume":"5","author":"Stabentheiner","year":"2010","journal-title":"PLoS ONE"},{"key":"ref_5","doi-asserted-by":"crossref","unstructured":"Seeley, T.D. (1985). Honeybee Ecology. A Study of Adaptation in Social Life, Princeton University Press.","DOI":"10.1515\/9781400857876"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"7343","DOI":"10.1073\/pnas.1232346100","article-title":"Behavioral performance in adult honey bees is influenced by the temperature experienced during their pupal development","volume":"100","author":"Tautz","year":"2003","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"4268","DOI":"10.1073\/pnas.0400773101","article-title":"Synaptic organization in the adult honey bee brain is influenced by brood-temperature control during pupal development","volume":"101","author":"Groh","year":"2004","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1121","DOI":"10.1007\/s00359-005-0035-z","article-title":"The effects of rearing temperature on developmental stability and learning and memory in the honey bee, Apis mellifera","volume":"191","author":"Jones","year":"2005","journal-title":"J. Comp. Physiol. A Neuroethol. Sens. Neural Behav."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"214","DOI":"10.1016\/j.jtherbio.2018.04.003","article-title":"Developmental stability, age at onset of foraging and longevity of Africanized honey bees (Apis mellifera L.) under heat stress (Hymenoptera: Apidae)","volume":"74","author":"Medina","year":"2018","journal-title":"J. Therm. Biol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"458","DOI":"10.1080\/00218839.2017.1412575","article-title":"Low temperature exposure (20 \u00b0C) during the sealed brood stage induces abnormal venation of honey bee wings","volume":"57","author":"Zhu","year":"2018","journal-title":"J. Apic. Res."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"673","DOI":"10.1007\/s00359-009-0442-7","article-title":"Pupal developmental temperature and behavioral specialization of honeybee workers (Apis mellifera L.)","volume":"195","author":"Becher","year":"2009","journal-title":"J. Comp. Physiol. A Neuroethol. Sens. Neural Behav."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"52","DOI":"10.3896\/IBRA.1.49.1.07","article-title":"Influence of brood rearing temperature on honey bee development and susceptibility to poisoning by pesticides","volume":"49","author":"Medrzycki","year":"2010","journal-title":"J. Apic. Res."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"96","DOI":"10.3896\/IBRA.1.52.2.19","article-title":"The effect of brood incubation temperature on the reproductive value of honey bee (Apis mellifera) drones","volume":"52","year":"2013","journal-title":"J. Apic. Res."},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Wang, Q., Xu, X., Zhu, X., Chen, L., Zhou, S., Huang, Z.-Y., and Zheng, B. (2016). Low-temperature stress during capped brood stage increases pupal mortality, misorientation and adult mortality in honey bees. PLoS ONE, 11.","DOI":"10.1371\/journal.pone.0154547"},{"key":"ref_15","unstructured":"Van der Laan, P.A. (1966). The effect of temperature on the pathogenicity of the fungus, Ascosphaera apis, for larvae of the honey bee, Apis mellifera. Insect Pathology and Microbial Control, North Holland Publishing Co."},{"key":"ref_16","unstructured":"Morse, R.A., and Flottum, K. (1997). Fungi. Honey Bee Pests, Predators and Diseases, AI Root Company."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"20","DOI":"10.1016\/j.jip.2009.06.018","article-title":"Chalkbrood disease in honey bees","volume":"103","author":"Aronstein","year":"2010","journal-title":"J. Invertebr. Pathol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"185","DOI":"10.1051\/apido:19960401","article-title":"Effect of temperature and humidity of sealed brood on chalkbrood development under controlled conditions","volume":"27","author":"Flores","year":"1996","journal-title":"Apidologie"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"200","DOI":"10.1016\/j.vetmic.2010.10.001","article-title":"Temperature dependent virulence of obligate and facultative fungal pathogens of honeybee brood","volume":"149","author":"Vojvodic","year":"2011","journal-title":"Vet. Microbiol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"229","DOI":"10.1007\/s001140050709","article-title":"Fever in honeybee colonies","volume":"87","author":"Starks","year":"2000","journal-title":"Naturwissenschaften"},{"key":"ref_21","first-page":"185","article-title":"Social benefits require a community: The influence of colony size on behavioral immunity in honey bees","volume":"27","author":"Bonoan","year":"2020","journal-title":"Apidologie"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"789","DOI":"10.3390\/insects3030789","article-title":"Behavioral immunity in insects","volume":"3","year":"2012","journal-title":"Insects"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"693","DOI":"10.1016\/j.cub.2007.06.008","article-title":"Social immunity","volume":"17","author":"Cremer","year":"2007","journal-title":"Curr. Biol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"663","DOI":"10.1093\/beheco\/arq070","article-title":"Personal immunity versus social immunity","volume":"21","author":"Cotter","year":"2010","journal-title":"Behav. Ecol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"20140102","DOI":"10.1098\/rstb.2014.0102","article-title":"Social immunity and the evolution of group living in insects","volume":"370","author":"Meunier","year":"2015","journal-title":"Philos. Trans. R. Soc. B"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"458","DOI":"10.1016\/j.cub.2019.03.035","article-title":"Social immunity in insects","volume":"29","author":"Cremer","year":"2019","journal-title":"Curr. Biol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"555","DOI":"10.1051\/apido:2001103","article-title":"Resistance to American foulbrood disease by honey bee colonies Apis mellifera bred for hygienic behavior","volume":"32","author":"Spivak","year":"2001","journal-title":"Apidologie"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"1799","DOI":"10.1073\/pnas.0333979100","article-title":"Social exploitation of vitellogenin","volume":"100","author":"Amdam","year":"2003","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_29","first-page":"527","article-title":"Impact of food availability, pathogen exposure, and genetic diversity on thermoregulation in honey bees (Apis mellifera)","volume":"27","author":"Foo","year":"2017","journal-title":"J. Insect Behav."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"335","DOI":"10.1038\/nri3843","article-title":"Fever and the thermal regulation of immunity: The immune system feels the heat","volume":"15","author":"Evans","year":"2015","journal-title":"Nat. Rev. Immunol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"691","DOI":"10.1080\/00218839.2020.1769276","article-title":"Effect of the own vs. foreign colony odor on daily shifts in olfactory and thermal preference and metabolic rate of the honey bee (Apis mellifera) workers","volume":"59","author":"Grodzicki","year":"2020","journal-title":"J. Apic. Res."},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Doublet, V., Poeschl, Y., Gogo-D\u00f6ring, A., Alaux, C., Annoscia, D., Aurori, C., Barribeau, S.M., Bedoya-Reina, O.C., Brown, M.J.F., and Bull, J.C. (2017). Unity in defence: Honeybee workers exhibit conserved molecular responses to diverse pathogens. BMC Genom., 18.","DOI":"10.1186\/s12864-017-3624-7"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"545","DOI":"10.1093\/icb\/ict004","article-title":"Cross-tolerance and cross-talk in the cold: Relating low temperatures to desiccation and immune stress in insects","volume":"53","author":"Sinclair","year":"2013","journal-title":"Integr. Comp. Biol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"408","DOI":"10.1016\/j.dci.2018.03.015","article-title":"Toll immune signal activates cellular immune response via eicosanoids","volume":"84","author":"Shafeeq","year":"2018","journal-title":"Dev. Comp. Immunol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"183","DOI":"10.1002\/arch.10081","article-title":"Eicosanoid involvement in the regulation of behavioral fever in the desert locust, Schistocerca gregaria","volume":"52","author":"Bundey","year":"2003","journal-title":"Arch. Insect Biochem. Physiol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"96","DOI":"10.1016\/j.jtherbio.2016.12.002","article-title":"Temperature stress and insect immunity","volume":"68","author":"Wojda","year":"2017","journal-title":"J. Therm. Biol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"130","DOI":"10.1016\/j.dci.2017.12.005","article-title":"Eicosanoid-mediated immunity in insects","volume":"83","author":"Kim","year":"2018","journal-title":"Dev. Comp. Immunol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"8850","DOI":"10.1038\/s41598-017-09159-4","article-title":"The heat shock response and humoral immune response are mutually antagonistic in honey bees","volume":"7","author":"McKinstry","year":"2017","journal-title":"Sci. Rep."},{"key":"ref_39","doi-asserted-by":"crossref","unstructured":"McMenamin, A.J., Daughenbaugh, K.F., and Flenniken, M.L. (2020). The heat shock response in the Western honey bee (Apis Mellifera) is antiviral. Viruses, 12.","DOI":"10.3390\/v12020245"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"1487","DOI":"10.1017\/S0031182010000235","article-title":"Behavioural fever in infected honeybees: Parasitic manipulation or coincidental benefit?","volume":"137","author":"Campbell","year":"2010","journal-title":"Parasitology"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"2554","DOI":"10.1128\/AEM.02908-08","article-title":"Effect of temperature on the biotic potential of honeybee microsporidia","volume":"75","author":"Meana","year":"2009","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"360","DOI":"10.1111\/j.1439-0310.1996.tb01132.x","article-title":"Effect of foraging distance on the thermal behaviour of honeybees during dancing, walking and trophallaxis","volume":"102","author":"Stabentheiner","year":"1996","journal-title":"Ethology"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"1653","DOI":"10.1242\/jeb.204.9.1653","article-title":"Changes in the thoracic temperature of honeybees while receiving nectar from foragers collecting at different reward rates","volume":"204","author":"Farina","year":"2001","journal-title":"J. Exp. Biol."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"36","DOI":"10.1007\/s003600050045","article-title":"Oxygen consumption in the foraging honeybee depends on the reward rate at the food source","volume":"167","author":"Moffatt","year":"1997","journal-title":"J. Comp. Physiol. B"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"4185","DOI":"10.1242\/jeb.02528","article-title":"Hot bumble bees at good food: Thoracic temperature of feeding Bombus wilmattae foragers is tuned to sugar concentration","volume":"209","author":"Nieh","year":"2006","journal-title":"J. Exp. Biol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"65","DOI":"10.1007\/BF00688889","article-title":"Colonial thermoregulation in honey bees (Apis mellifera)","volume":"2148","author":"Kronenberg","year":"1982","journal-title":"J. Comp. Physiol."}],"container-title":["Insects"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2075-4450\/11\/8\/528\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T10:00:06Z","timestamp":1760176806000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2075-4450\/11\/8\/528"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,8,13]]},"references-count":46,"journal-issue":{"issue":"8","published-online":{"date-parts":[[2020,8]]}},"alternative-id":["insects11080528"],"URL":"https:\/\/doi.org\/10.3390\/insects11080528","relation":{},"ISSN":["2075-4450"],"issn-type":[{"value":"2075-4450","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,8,13]]}}}