Skip to main content

The survival consequences of grooming in the honey bee Apis mellifera

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.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2

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

    Article  CAS  Google Scholar 

  • Aumeier P (2001) Bioassay for grooming effectiveness towards Varroa destructor mites in Africanized and Carniolan honey bees. Apidologie 32:81–90

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Barron AB, Maleszka R, Vander Meer RK, Robinson GE (2007) Octopamine modulates honey bee dance language behavior. Proc Natl Acad Sci 104:1703–1707

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Boecking O, Spivak M (1999) Behavioral defenses of honey bees against Varroa jacobsoni Oud. Apidologie 30:141–158

    Article  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Bozic J, Valentincic T (1995) Quantitative analysis of social grooming behavior of the honey bee Apis mellifera carnica. Apidologie 26:141–147

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Chen P, Hong W (2018) Neural circuit mechanisms of social behavior. Neuron 98:16–30

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 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

    PubMed  PubMed Central  Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Cremer S, Armitage SA, Schmid-Hempel P (2007) Social immunity. Curr Biol 17:R693-702

    CAS  PubMed  Article  Google Scholar 

  • Cremer S, Pull CD, Furst MA (2018) Social immunity: emergence and evolution of colony-level disease protection. Annu Rev Entomol 63:105–123

    CAS  PubMed  Article  Google Scholar 

  • DeVries AC, Glasper ER, Detillion CE (2003) Social modulation of stress responses. Physiol Behav 79:399–407

    CAS  PubMed  Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Evans JD, Spivak M (2010) Socialized medicine: individual and communal disease barriers in honey bees. J Invertebr Pathol 103(Suppl 1):S62-72

    PubMed  Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Golenda CF, Forgash AJ (1986) Grooming behavior in response to fenvalerate treatment in pyrethroid-resistant house flies. Entomol Exp Appl 40:169–175

    CAS  Article  Google Scholar 

  • Grozinger CM, Flenniken ML (2019) Bee viruses: ecology, pathogenicity, and impacts. Annu Rev Entomol 64:205–226

    CAS  PubMed  Article  Google Scholar 

  • 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

    PubMed  Article  Google Scholar 

  • 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

    PubMed  PubMed Central  Article  Google Scholar 

  • 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

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • James RR, Xu J (2012) Mechanisms by which pesticides affect insect immunity. J Invertebr Pathol 109:175–182

    CAS  PubMed  Article  Google Scholar 

  • 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

    CAS  PubMed  Article  Google Scholar 

  • 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

    CAS  Article  Google Scholar 

  • Kucharski R, Maleszka R (2003) Transcriptional profiling reveals multifunctional roles for transferrin in the honeybee Apis mellifera. J Insect Sci 3:27–34

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Kuszewska K, Woyciechowski M (2014) Risky robbing is a job for short-lived and infected worker honeybees. Apidologie 45:537–544

    Article  Google Scholar 

  • Land BB, Seeley TD (2004) The grooming invitation dance of the honey bee. Ethology 110:1–10

    Article  Google Scholar 

  • Li T, Wang P, Wang SC, Wang YF (2016) Approaches mediating oxytocin regulation of the immune system. Front Immunol 7:693

    PubMed  Google Scholar 

  • 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

    PubMed  Article  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Nicholls E, Hempel de Ibarra N, Nicolson S (2016) Assessment of pollen rewards by foraging bees. Funct Ecol 31:76–87

    Article  Google Scholar 

  • Pettis J, Pankiw T (1998) Grooming behavior by Apis mellifera L. in the presence of Acarapis woodi (Rennie) (Acari: Tarsonemidae). Apidologie 29:241–253

    Article  Google Scholar 

  • Pritchard DJ (2016) Grooming by honey bees as a component of varroa resistant behavior. J Apic Res 55:38–48

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • Root-Bernstein M (2010) Displacement activities during the honeybee transition from waggle dance to foraging. Anim Behav 79:935–938

    Article  Google Scholar 

  • 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

    CAS  PubMed  Article  Google Scholar 

  • 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

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Silk JB, Alberts SC, Altmann J (2003) Social bonds of female baboons enhance infant survival. Science 302:1231–1234

    CAS  PubMed  Article  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • Sovik E, Cornish JL, Barron AB (2013) Cocaine tolerance in honey bees. PLoS ONE 8:e64920

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Stroeymeyt N, Casillas-Perez B, Cremer S (2014) Organizational immunity in social insects. Curr Opin Insect Sci 5:1–15

    PubMed  Article  Google Scholar 

  • Troisi A (2002) Displacement activities as a behavioral measure of stress in nonhuman primates and human subjects. Stress 5:47–54

    PubMed  Article  Google Scholar 

  • 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

    PubMed  PubMed Central  Article  Google Scholar 

  • Winston ML (1987) The biology of the honey bee. Harvard University Press, Cambridge

    Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 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

    CAS  PubMed  Article  Google Scholar 

  • Zhukovskaya M, Yanagawa A, Forschler BT (2013) Grooming behavior as a mechanism of insect disease defense. Insects 4:609–630

    PubMed  PubMed Central  Article  Google Scholar 

Download references

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).

Author information

Authors and Affiliations

Authors

Contributions

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.

Corresponding author

Correspondence to C. C. Rittschof.

Ethics declarations

Conflict of interest

Authors declare no competing interests.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 53 KB)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00040-022-00868-2

Keywords

  • Social immunity
  • Varroa mite
  • Allogrooming