Skip to main content
Log in

Do Bumble Bees Produce Brood Pheromones?

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

Reproductive division of labor, a defining feature of social insects, is often regulated by a combination of behavioral and chemical means. It is hypothesized that behavioral interactions play a more important role in regulating reproduction of primitive eusocial species, while pheromones are typically used by large sized, advanced eusocial species. Here we examined if worker reproduction in the primitively eusocial species Bombus impatiens is regulated by brood pheromones. We recently demonstrated that worker egg laying in this species is inhibited by young larvae and triggered by pupae. However, the mechanism by which the brood communicates its presence and whether brood or hunger pheromones are involved remain unknown. We found that workers were behaviorally attracted to pupae over larvae or control in a choice experiment, in line with their reproductive interests. However, odors from larvae or pupae were insufficient to inhibit worker reproduction. We further show that the youngest larvae are particularly vulnerable to starvation, however, despite a slight attraction and fewer eggs laid by workers in the presence of starved compared with fed larvae, these effects were insignificant. Our study demonstrates that workers can differentiate between larvae and pupae, but not between starved and fed larvae based on olfactory information. However, these signals alone do not explain the reduction in worker egg laying previously found. Bumble bee workers may use information from multiple sources or rely solely on behavioral interactions with brood and other females to make decisions about reproduction, in line with their small colony size and simple social organization.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Alaux C, Jaisson P, Hefetz A (2005) Reproductive decision-making in semelparous colonies of the bumblebee Bombus terrestris. Behav Ecol Sociobiol 59:270–277

    Article  Google Scholar 

  • Amsalem E, Hefetz A (2010) The appeasement effect of sterility signaling in dominance contests among Bombus terrestris workers. Behav Ecol Sociobiol 64:1685–1694

    Article  Google Scholar 

  • Amsalem E, Twele R, Francke W, Hefetz A. (2009) Reproductive competition in the bumble-bee Bombus terrestris: do workers advertise sterility? Proc R Soc B 276:1295–1304

  • Amsalem E, Kiefer J, Schulz S, Hefetz A (2014) The effect of caste and reproductive state on the chemistry of the cephalic labial glands secretion of Bombus terrestris. J Chem Ecol 40:900–912

    Article  CAS  PubMed  Google Scholar 

  • Amsalem E, Grozinger CM, Padilla M, Hefetz A (2015a) The physiological and genomic bases of bumble bee social behaviour. In: Amro Z, Clement FK (eds) genomics, physiology and behaviour of social insects, Academic Press, Adv In Insect Phys, 48:37–93

  • Amsalem E, Orlova M, Grozinger CM (2015b) A conserved class of queen pheromones? Re-evaluating the evidence in bumblebees (Bombus impatiens). Proc R Soc B Biol Sci 282:20151800

    Article  CAS  Google Scholar 

  • Amsalem E, Padilla M, Schreiber PM, Altman NS, Hefetz A, Grozinger CM (2017) Do bumble bee, Bombus impatiens, queens signal their reproductive and mating status to their workers? J Chem Ecol 43:563–572

    Article  CAS  PubMed  Google Scholar 

  • Beshers SN, Fewell JH (2001) Models of division of labor in social insects. Annu Rev Entomol 46:413–440

    Article  CAS  PubMed  Google Scholar 

  • Bhadra A, Mitra A, Deshpande SA, Chandrasekhar K, Naik DG, Hefetz A, Gadagkar R (2010) Regulation of reproduction in the primitively eusocial wasp Ropalidia marginata: on the trail of the queen pheromone. J Chem Ecol 36:424–431

    Article  CAS  PubMed  Google Scholar 

  • Bigley WS, Vinson SB (1975) Characterization of a brood pheromone isolated from the sexual brood of the imported fire ant, Solenopsis invicta. Ann Entomol Soc Am 68:301–304

    Article  CAS  Google Scholar 

  • Bloch G, Hefetz A (1999) Reevaluation of the role of mandibular glands in regulation of reproduction in bumblebee colonies. J Chem Ecol 25:881–896

    Article  CAS  Google Scholar 

  • Blomquist GJ, Bagnères A-G (2010) Insect hydrocarbons: biology, biochemistry, and chemical ecology. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Boer SPA, Duchateau MJHM (2006) A larval hunger signal in the bumblebee Bombus terrestris. Insect Soc 53:369–373

    Article  Google Scholar 

  • Cnaani J, Schmid-Hempel R, Schmidt JO (2002) Colony development, larval development and worker reproduction in Bombus impatiens cresson. Insect Soc 49:164–170

    Article  Google Scholar 

  • Duchateau MJ, Velthuis HHW (1988) Development and reproductive strategies in Bombus terrestris colonies. Behavior 107:186–207

    Article  Google Scholar 

  • Engel KC, Stokl J, Schweizer R, Vogel H, Ayasse M, Ruther J, Steiger S (2016) A hormone-related female anti-aphrodisiac signals temporary infertility and causes sexual abstinence to synchronize parental care. Nat Commun 7:11035

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fletcher DJC, Ross KG (1985) Regulation of reproduction in eusocial hymenoptera. Annu Rev Entomol 30:319–343

    Article  Google Scholar 

  • Funaro CF, Boroczky K, Vargo EL, Schal C (2018) Identification of a queen and king recognition pheromone in the subterranean termite reticulitermes flavipes. Proc Natl Acad Sci U S A 115:3888–3893

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Godfray HCJ (1991) Signalling of need by offspring to their parents. Nature 352:328–330

    Article  Google Scholar 

  • Haig D (1990) Brood reduction and optimal parental investment when offpsring differ in quality. Am Nat 136:550–556

    Article  Google Scholar 

  • He XJ, Zhang XC, Jiang WJ, Barron AB, Zhang JH, Zeng ZJ (2016) Starving honey bee (apis mellifera) larvae signal pheromonally to worker bees. Sci Rep 6:22359

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Holldobler B, Wilson EO (1983) Queen control in colonies of weaver ants (hymenoptera: Fornicidae). Ann Entomol Soc Am 76:235–238

    Article  Google Scholar 

  • Hoover SE, Keeling CI, Winston ML, Slessor KN (2003) The effect of queen pheromones on worker honey bee ovary development. Naturwissenschaften 90:477–480

    Article  CAS  PubMed  Google Scholar 

  • Jandt JM, Tibbetts EA, Toth AL (2013) Polistes paper wasps: a model genus for the study of social dominance hierarchies. Insect Soc 61:11–27

    Article  Google Scholar 

  • Keller L, Nonacs P (1993) The role of queen pheromones in social insects: queen control or queen signal? Anim Behav 45:787–794

    Article  Google Scholar 

  • Kilner R, Johnstone RA (1997) Begging the question: are offspring solicitation behaviours signals of need? Trends Ecol Evol 12:11–15

    Article  CAS  PubMed  Google Scholar 

  • Kocher SD, Grozinger CM (2011) Cooperation, conflict, and the evolution of queen pheromones. J Chem Ecol 37:1263–1275

    Article  CAS  PubMed  Google Scholar 

  • Le Conte Y, Hefetz A (2008) Primer pheromones in social hymenoptera. Annu Rev Entomol 53:523–542

    Article  CAS  PubMed  Google Scholar 

  • Le Conte Y, Mohammedi A, Robinson GE (2001) Primer effects of a brood pheromone on honeybee behavioural development. Proc Biol Sci 268:163–168

    Article  PubMed  PubMed Central  Google Scholar 

  • Liebig J, Peeters C, Holldobler B (1999) Worker policing limits the number of reproductives in a ponerine ant. Proc R Soc Lond B 266:1865–1870

    Article  Google Scholar 

  • Liebig J, Eliyahu D, Brent CS (2009) Cuticular hydrocarbon profiles indicate reproductive status in the termite Zootermopsis nevadensis. Behav Ecol Sociobiol 63:1799–1807

    Article  Google Scholar 

  • Lofgren CS, Glancey BM, Glover A, Rocca J, Tumlinson J (1983) Behavior of workers of Solenopsis invicta (hymenoptera: Formicidae) to the queen recognition pheromone: laboratory studies with an olfactometer and surrogate queens. Ann Entomol Soc Am 76:44–50

    Article  Google Scholar 

  • Maisonnasse A, Lenoir JC, Beslay D, Crauser D, Le Conte Y (2010) E-beta-ocimene, a volatile brood pheromone involved in social regulation in the honey bee colony (Apis mellifera). PLoS One 5:e13531

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matsuura K, Himuro C, Yokoi T, Yamamoto Y, Vargo EL, Keller L (2010) Identification of a pheromone regulating caste differentiation in termites. Proc Natl Acad Sci U S A 107:12963–12968

    Article  PubMed  PubMed Central  Google Scholar 

  • Melgarejo V, Wilson Rankin EE, Loope KJ (2018) Do queen cuticular hydrocarbons inhibit worker reproduction in Bombus impatiens? Insect Soc 65:601–608

    Article  Google Scholar 

  • Michener CD (1974) The social behavior of the bees. Harvard University Press, Cambridge

    Google Scholar 

  • Monnin T, Jones G, Ratnieks FLW, Beard R (2002) Pretender punishment induced by chemical signaling in a queenless ant. Nature 419:61–65

    Article  CAS  PubMed  Google Scholar 

  • Naug D (2009) Structure and resilience of the social network in an insect colony as a function of colony size. Behav Ecol Sociobiol 63:1023–1028

    Article  Google Scholar 

  • Noonan KC (2010) Recognition of queen larvae by worker honey bees (Apis mellifera). Ethology 73:295–306

    Article  Google Scholar 

  • Nunes TM et al (2014) Queen signals in a stingless bee: suppression of worker ovary activation and spatial distribution of active compounds. Sci Rep 4:7449

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oi CA, van Zweden JS, Oliveira RC, Van Oystaeyen A, Nascimento FS, Wenseleers T (2015) The origin and evolution of social insect queen pheromones: novel hypotheses and outstanding problems. Bioessays 37:808–821

    Article  CAS  PubMed  Google Scholar 

  • Orlova M, Amsalem E (2019) Context matters: plasticity in response to pheromones regulating reproduction and collective behavior in social hymenoptera. Curr Opin Insect Sci 35:69–76

    Article  PubMed  Google Scholar 

  • Padilla M, Amsalem E, Altman N, Hefetz A, Grozinger CM (2016) Chemical communication is not sufficient to explain reproductive inhibition in the bumblebee Bombus impatiens. R Soc Open Sci 3:160576

    Article  PubMed  PubMed Central  Google Scholar 

  • Page RE, Robinson GE, Fondrk MK (1989) Genetic specialists, kin recognition and nepotism in honey-bee colonies. Nature 338:576–579

    Article  Google Scholar 

  • Peeters C, Liebig J (2009) Fertility signaling as a general mechanism of regulating reproductive division of labor in ants. In: Gadau J, Fewell J (eds) In organization of insect societies: from genome to sociocomplexity. Harvard University Press, Cambridge

    Google Scholar 

  • Pereboom JJM, Duchateau MJ, Velthuis HHW (2003) The organisation of larval feeding in bumblebees (hymenoptera, apidae) and its significance to caste differentiation. Insect Soc 50:127–133

    Article  Google Scholar 

  • Premnath S, Sinha A, Gadagkar R (1995) Regulation of worker activity in a primitively eusocial wasp, Ropalidia marginata. Behav Ecol 6:117–123

    Article  Google Scholar 

  • Premnath S, Sinha A, Gadagkar R (1996) Dominance relationship in the establishment of reproductive division of labour in a primitively eusocial wasp (Ropalidia marginata). Behav Ecol Sociobiol 39:125–132

    Article  Google Scholar 

  • Queller David C (1994) Extended parental care and the origin of eusociality. Proc R Soc Lond Ser B Biol Sci 256:105–111

    Article  Google Scholar 

  • Ratnieks FLW, Visscher PK (1989) Worker policing in the honeybee. Nature 342:796–797

    Article  Google Scholar 

  • Schultner E, Oettler J, Helantera H (2017) The role of brood in eusocial hymenoptera. Q Rev Biol 92:39–78

    Article  PubMed  Google Scholar 

  • Smith AA, Liebig J (2017) The evolution of cuticular fertility signals in eusocial insects. Curr Opin Insect Sci 22:79–84

    Article  PubMed  Google Scholar 

  • Starkey J, Brown A, Amsalem E (2019) The road to sociality: brood regulation of worker reproduction in the simple eusocial bee Bombus impatiens. Anim Behav 154:57–65

    Article  Google Scholar 

  • Trivers RL, Hare H (1976) Haplodiploidy and the evolution of the social insects. Science 191:249–263

    Article  CAS  PubMed  Google Scholar 

  • Ulrich Y, Burns D, Libbrecht R, Kronauer DJ (2016) Ant larvae regulate worker foraging behavior and ovarian activity in a dose-dependent manner. Behav Ecol Sociobiol 70:1011–1018

    Article  PubMed  Google Scholar 

  • Winston ML, Slessor KN, Willis LG, Naumann K, Higo HA, Wyborn MH, Kaminski LA (1989) The influence of queen mandibular pheromones on worker attraction to swarm clusters and inhibition of queen rearing in the honey bee (Apis mellifera l.). Insect Soc 36:15–27

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Etya Amsalem.

Electronic supplementary material

ESM 1

(DOCX 9620 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Starkey, J., Derstine, N. & Amsalem, E. Do Bumble Bees Produce Brood Pheromones?. J Chem Ecol 45, 725–734 (2019). https://doi.org/10.1007/s10886-019-01101-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-019-01101-4

Keywords

Navigation