Abstract
In social animals, disease management behaviors such as grooming occur in response to diverse stimuli, making it difficult to interpret the evolution and function of these phenotypes. The honey bee has a grooming repertoire that includes self-directed behaviors and allogrooming from nestmates. Many stimuli provoke these behaviors, and their impacts on individual and colony survivorship are unclear. We evaluated the effects of two different stressors on grooming frequencies and survivorship. We found that self-grooming frequency is activated in distinct ways in response to pathogen infection, pesticide treatment, and social context. Moreover, self-grooming frequency predicts individual survival. Allogrooming interactions were less common and did not predict individual survival. The honey bee highlights the difficulty inherent in interpreting the evolution and function of grooming interactions in highly social species.
References
Al Naggar Y, Paxton RJ (2020) Mode of transmission determines the virulence of black queen cell virus in adult honey bees, posing a future threat to bees and apiculture. Viruses 12:1–12
Aumeier P (2001) Bioassay for grooming effectiveness towards Varroa destructor mites in Africanized and Carniolan honey bees. Apidologie 32:81–90
Bąk B, Wilde J (2016) Grooming behavior by worker bees of various subspecies of honey bees to remove Varroa destructor mites. J Apic Res 54:207–215
Barron AB, Maleszka R, Vander Meer RK, Robinson GE (2007) Octopamine modulates honey bee dance language behavior. Proc Natl Acad Sci 104:1703–1707
Boecking O, Spivak M (1999) Behavioral defenses of honey bees against Varroa jacobsoni Oud. Apidologie 30:141–158
Boroczky K, Wada-Katsumata A, Batchelor D, Zhukovskaya M, Schal C (2013) Insects groom their antennae to enhance olfactory acuity. Proc Natl Acad Sci USA 110:3615–3620
Bozic J, Valentincic T (1995) Quantitative analysis of social grooming behavior of the honey bee Apis mellifera carnica. Apidologie 26:141–147
Carr HM, Palmer JH, Rittschof CC (2020) Honey bee aggression: evaluating causal links to disease-resistance traits and infection. Behav Ecol Sociobiol 74:1–14
Chen P, Hong W (2018) Neural circuit mechanisms of social behavior. Neuron 98:16–30
Cini A, Bordoni A, Cappa F, Petrocelli I, Pitzalis M, Iovinella I, Dani FR, Turillazzi S, Cervo R (2020) Increased immunocompetence and network centrality of allogroomer workers suggest a link between individual and social immunity in honeybees. Sci Rep 10:8928
Cinini SM, Barnabe GF, Galvao-Coelho N, de Medeiros MA, Perez-Mendes P, Sousa MB, Covolan L, Mello LE (2014) Social isolation disrupts hippocampal neurogenesis in young non-human primates. Front Neurosci 8:45
Corby-Harris V, Bowsher JH, Carr-Markell M, Carroll MJ, Centrella M, Cook SC, Couvillon M, DeGrandi-Hoffman G, Dolezal A, Jones JC, Mogren CL, Otto CRV, Lau P, Rangel J, Schürch R, St. Clair A (2018) Emerging themes from the ESA symposium entitled “Pollinator Nutrition: Lessons from Bees at Individual to Landscape Levels.” Bee World 96:3–9
Cox RL, Wilson WT (1984) Effects of permethrin on the behavior of individually tagged honey bees, Apis mellifera L. (Hymenoptera: Apidae). Environ Entomol 13:375–378
Cremer S, Armitage SA, Schmid-Hempel P (2007) Social immunity. Curr Biol 17:R693-702
Cremer S, Pull CD, Furst MA (2018) Social immunity: emergence and evolution of colony-level disease protection. Annu Rev Entomol 63:105–123
DeVries AC, Glasper ER, Detillion CE (2003) Social modulation of stress responses. Physiol Behav 79:399–407
Eads DA, Biggins DE, Eads SL, Ebensperger L (2017) Grooming behaviors of black-tailed prairie dogs are influenced by flea parasitism, conspecifics, and proximity to refuge. Ethology 123:924–932
Evans JD, Spivak M (2010) Socialized medicine: individual and communal disease barriers in honey bees. J Invertebr Pathol 103(Suppl 1):S62-72
Fefferman NH, Traniello JFA, Rosengaus RB, Calleri DV (2006) Disease prevention and resistance in social insects: modeling the survival consequences of immunity, hygienic behavior, and colony organization. Behav Ecol Sociobiol 61:565–577
Golenda CF, Forgash AJ (1986) Grooming behavior in response to fenvalerate treatment in pyrethroid-resistant house flies. Entomol Exp Appl 40:169–175
Grozinger CM, Flenniken ML (2019) Bee viruses: ecology, pathogenicity, and impacts. Annu Rev Entomol 64:205–226
Guzman-Novoa E, Emsen B, Unger P, Espinosa-Montano LG, Petukhova T (2012) Genotypic variability and relationships between mite infestation levels, mite damage, grooming intensity, and removal of Varroa destructor mites in selected strains of worker honey bees (Apis mellifera L.). J Invertebr Pathol 110:314–320
Hamiduzzaman MM, Emsen B, Hunt GJ, Subramanyam S, Williams CE, Tsuruda JM, Guzman-Novoa E (2017) Differential gene expression associated with honey bee grooming behavior in response to varroa mites. Behav Genet 47:335–344
Hewlett SE, Delahunt Smoleniec JD, Wareham DM, Pyne TM, Barron AB (2018) Biogenic amine modulation of honey bee sociability and nestmate affiliation. PLoS ONE 13:e0205686
Huang Z, Robinson GE (1992) Honeybee colony integration: worker-worker interactions mediate hormonally regulated plasticity in division of labor. Proc Natl Acad Sci 89:11726–11729
James RR, Xu J (2012) Mechanisms by which pesticides affect insect immunity. J Invertebr Pathol 109:175–182
Kalueff AV, Stewart AM, Song C, Berridge KC, Graybiel AM, Fentress JC (2016) Neurobiology of rodent self-grooming and its value for translational neuroscience. Nat Rev Neurosci 17:45–59
Kovac D, Maschwitz U (1990) Secretion-grooming in aquatic beetles (Hydradephaga): a chemical protection against contamination of the hydrofuge respiratory region. Chemoecology 1:131–138
Kucharski R, Maleszka R (2003) Transcriptional profiling reveals multifunctional roles for transferrin in the honeybee Apis mellifera. J Insect Sci 3:27–34
Kuszewska K, Woyciechowski M (2014) Risky robbing is a job for short-lived and infected worker honeybees. Apidologie 45:537–544
Land BB, Seeley TD (2004) The grooming invitation dance of the honey bee. Ethology 110:1–10
Li T, Wang P, Wang SC, Wang YF (2016) Approaches mediating oxytocin regulation of the immune system. Front Immunol 7:693
Li Y, Hassett AL, Seng JS (2019) Exploring the mutual regulation between oxytocin and cortisol as a marker of resilience. Arch Psychiatr Nurs 33:164–173
Li-Byarlay H, Rittschof CC, Massey JH, Pittendrigh BR, Robinson GE (2014) Socially responsive effects of brain oxidative metabolism on aggression. Proc Natl Acad Sci USA 111:12533–12537
Nicholls E, Hempel de Ibarra N, Nicolson S (2016) Assessment of pollen rewards by foraging bees. Funct Ecol 31:76–87
Pettis J, Pankiw T (1998) Grooming behavior by Apis mellifera L. in the presence of Acarapis woodi (Rennie) (Acari: Tarsonemidae). Apidologie 29:241–253
Pritchard DJ (2016) Grooming by honey bees as a component of varroa resistant behavior. J Apic Res 55:38–48
Richard FJ, Holt HL, Grozinger CM (2012) Effects of immunostimulation on social behavior, chemical communication and genome-wide gene expression in honey bee workers (Apis mellifera). BMC Genom 13:1–17
Rittschof CC, Rubin BER, Palmer JH (2019) The transcriptomic signature of low aggression in honey bees resembles a response to infection. BMC Genom 20:1029
Rittschof CC, Vekaria HJ, Palmer JH, Sullivan PG (2018) Brain mitochondrial bioenergetics change with rapid and prolonged shifts in aggression in the honey bee, Apis mellifera. J Exp Biol 221:1–10
Root-Bernstein M (2010) Displacement activities during the honeybee transition from waggle dance to foraging. Anim Behav 79:935–938
Rueppell O, Hayworth MK, Ross NP (2010) Altruistic self-removal of health-compromised honey bee workers from their hive. J Evol Biol 23:1538–1546
Russo RM, Liendo MC, Landi L, Pietronave H, Merke J, Fain H, Muntaabski I, Palacio MA, Rodríguez GA, Lanzavecchia SB, Scannapieco AC (2020) Grooming behavior in naturally varroa-resistant Apis mellifera colonies from North-Central Argentina. Front Ecol Evol 8
Schweinfurth MK, Stieger B, Taborsky M (2017) Experimental evidence for reciprocity in allogrooming among wild-type Norway rats. Sci Rep 7:4010
Silk JB, Alberts SC, Altmann J (2003) Social bonds of female baboons enhance infant survival. Science 302:1231–1234
Smith J, Cleare XL, Given K, Li-Byarlay H (2021) Morphological changes in the mandibles accompany the defensive behavior of Indiana mite biting honey bees against Varroa destructor. Front Ecol Evol 9:1–9
Smolinksy AN, Bergner CL, LaPorte JL, Kalueff AV (2009) Analysis of grooming behavior and its utility in studying animal stress, anxiety, and depression. In: Gould TD (ed) Mood and anxiety related phenotypes in mice: characterization using behavioral tests. Humana Press, Totowa, pp 21–36
Sovik E, Cornish JL, Barron AB (2013) Cocaine tolerance in honey bees. PLoS ONE 8:e64920
Stroeymeyt N, Casillas-Perez B, Cremer S (2014) Organizational immunity in social insects. Curr Opin Insect Sci 5:1–15
Troisi A (2002) Displacement activities as a behavioral measure of stress in nonhuman primates and human subjects. Stress 5:47–54
Waddington KD, Rothenbuhler WC (1975) Behaviour associated with hairless-black syndrome of adult honeybees. J Apic Res 15:35–41
Walker TN, Hughes WO (2009) Adaptive social immunity in leaf-cutting ants. Biol Lett 5:446–448
Winston ML (1987) The biology of the honey bee. Harvard University Press, Cambridge
Yanagawa A, Fujiwara-Tsujii N, Akino T, Yoshimura T, Yanagawa T, Shimizu S (2012) Odor aversion and pathogen-removal efficiency in grooming behavior of the termite Coptotermes formosanus. PLoS ONE 7:e47412
Yang X, Cox-Foster D (2007) Effects of parasitization by Varroa destructor on survivorship and physiological traits of Apis mellifera in correlation with viral incidence and microbial challenge. Parasitology 134:405–412
Zhukovskaya M, Yanagawa A, Forschler BT (2013) Grooming behavior as a mechanism of insect disease defense. Insects 4:609–630
Acknowledgements
We thank Jimmy Harrison for help maintaining honey bee colonies.
Funding
This work was supported by a University of Kentucky Office of Undergraduate Research Sustainability Research Fellowship (awarded to A. M. F.), the National Institute of Food and Agriculture Hatch Program (1012993), the Foundation for Food and Agriculture Research (549049), and the National Science Foundation (IOS-2045901).
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AMF collected data and wrote the manuscript, RRW designed experiment, collected data, and edited the manuscript, MV designed figures and wrote the manuscript, CCR designed the experiment, analyzed data, and wrote the manuscript.
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Foose, A.M., Westwick, R.R., Vengarai, M. et al. The survival consequences of grooming in the honey bee Apis mellifera. Insect. Soc. 69, 279–287 (2022). https://doi.org/10.1007/s00040-022-00868-2
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DOI: https://doi.org/10.1007/s00040-022-00868-2