Advertisement

Behavioral Ecology and Sociobiology

, Volume 70, Issue 11, pp 1891–1900 | Cite as

Maternal manipulation of pollen provisions affects worker production in a small carpenter bee

  • Sarah P. Lawson
  • Krista N. Ciaccio
  • Sandra M. Rehan
Original Article

Abstract

Mothers play a key role in determining the body size, behavior, and fitness of offspring. Mothers of the small carpenter bee, Ceratina calcarata, provide smaller pollen balls to their first female offspring resulting in the development of a smaller female. This smaller female, known as the dwarf eldest daughter, is coerced to stay at the nest to forage and feed siblings as a worker. In order to better understand how this maternal manipulation leads to the physiological and behavioral differences observed in dwarf eldest daughters, we characterized and compared the quality of the pollen balls fed to theses females vs. other offspring. Our results confirm earlier studies reporting that there is a female-biased sex allocation in the first brood cell position and these daughters received mass provisions significantly smaller than other daughters. In addition to the smaller quantities of pollen provisioned, we found evidence for maternal control of the quality of pollen invested in the dwarf eldest daughters. Late brood cells receive pollen balls with significantly less floral diversity than early brood cells. This difference in floral diversity affects the protein content of the pollen balls; in that, older offspring receive less protein than their younger siblings. These results reveal that C. calcarata mothers manipulate not only the quantity but also the quality of the provision provided to her first offspring to create a small worker she is able to coerce to remain at the nest to help raise her siblings. This overlapping of generations and division of labor between mother and dwarf eldest daughter may represent the first steps in the evolution of highly social groups. One of the major transitions to the formation of highly social groups is division of labor. By manipulating resource availability to offspring, parents can force offspring to remain at the nest to serve as a worker leading to a division of labor between parent and offspring. In the small carpenter bee, C. calcarata, mothers provide their eldest daughter with less food resulting in a smaller adult body size. This dwarf eldest daughter (DED) does not have the opportunity to reproduce and serves only as a worker for the colony. In addition to overall reduced investment, we found that mothers also provide a different variety of pollen to her DED. By exploring the factors and mechanisms that influence maternal manipulation in a non-eusocial bee, we can begin to understand one of the major transitions in social group formation.

Keywords

Eusocial Pollen Foraging Floral diversity Protein content Maternal manipulation Ceratina calcarata 

Notes

Acknowledgments

We thank Sean Lombard, Nicholas Pizzi, Wyatt Shell, and Jacob Withee for their assistance with field collections and nest processing. This work was supported by NSF award no. 1456296 to SMR and award no. 1523664 to SPL. Additionally, this research was supported by the University of New Hampshire, the New Hampshire Agricultural Experiment Station, and the Tuttle Foundation funds to SMR.

Compliance with ethical standards

All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted. This article does not contain any studies with human participants performed by any of the authors.

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Alexander RD (1974) The evolution of social behavior. Annu Rev Ecol Syst 5:325–383CrossRefGoogle Scholar
  2. Amaya-Marquez M (2009) Floral constancy in bees, a revision of theories and a comparison with other pollinators. Rev Colomb Entomol 35:206–216Google Scholar
  3. Andersson M (1984) The evolution of eusociality. Annu Rev Ecol Syst 15:165–189CrossRefGoogle Scholar
  4. Behmer ST (2009) Insect herbivore nutrient regulation. Annu Rev Entomol 54:165–187CrossRefPubMedGoogle Scholar
  5. Brand N, Chapuisat M (2012) Born to be bee, fed to be worker? The caste system of a primitively eusocial insect. Front Zool 9:35CrossRefPubMedPubMedCentralGoogle Scholar
  6. Bray JR, Curtis JT (1957) An ordination of upland forest communities of southern Wisconsin. Ecol Monogr 27:325–349CrossRefGoogle Scholar
  7. Brodschneider R, Crailsheim K (2010) Nutrition and health in honey bees. Apidologie 41:278–294CrossRefGoogle Scholar
  8. Charnov EL (1978) Evolution of eusocial behavior: offspring choice or parental parasitism? J Theor Biol 75:451–465CrossRefPubMedGoogle Scholar
  9. Clarke MF (1984) Co-operative breeding by the Australian bell miner Manorina melanophrys Latham: a test of kin selection theory. Behav Ecol Sociobiol 14:137–146CrossRefGoogle Scholar
  10. Colwell RK (2013) EstimateS: statistical estimation of species richness and shared species from samples. Version 9. User’s Guide and application published at: http://purl.oclc.org/estimates
  11. Cook SM, Awmack CS, Murray DA, Williams IH (2003) Are honey bees’ foraging preferences affected by pollen amino acid composition? Ecol Entomol 28:622–627CrossRefGoogle Scholar
  12. Craig R (1979) Parental manipulation, kin selection, and the evolution of altruism. Evolution 33:319–334CrossRefGoogle Scholar
  13. Crespi BJ, Ragsdale JE (2000) A skew model for the evolution of sociality via manipulation: why it is better to be feared than loved. Proc R Soc B 267:821–828CrossRefPubMedPubMedCentralGoogle Scholar
  14. Day S (1990) The nutrient composition of honeybee-collected pollen in Otago, New Zealand. J Api Res 29:138–146CrossRefGoogle Scholar
  15. Delaplane KS, Dag A, Danka RG, Freitas BM, Garibaldi LA, Goodwin RM, Hormaza JI (2013) Standard methods for pollination research with Apis mellifera. In: Dietemann V, Ellis JD, Neumann P (eds) The COLOSS Beebook Volume II: standard methods for Apis mellifera research. J Apicultural ResGoogle Scholar
  16. Gadagkar R (1991) Belonogaster, Mischocyttarus, Parapolybia and independent-founding Ropalidia. In: Ross KG, Matthews RW (eds) The social biology of wasps. Cornell University Press, Ithaca, pp. 149–190Google Scholar
  17. Gadagkar R, Chandrashekara K, Chandran S, Bhagavan S (1991) Worker-brood genetic relatedness in a primitively eusocial wasp—a pedigree analysis. Naturwissenschaften 78:523–526CrossRefGoogle Scholar
  18. Genissel A, Aupinel P, Bressac C, Tasei JN, Chevrier C (2002) Influence of pollen origin on performance of Bombus terrestris micro-colonies. Entomol Exp Appl 104:329–336CrossRefGoogle Scholar
  19. Gilbert EF (1961) Phenology of sumacs. Am Midl Nat 66:286–300CrossRefGoogle Scholar
  20. Gleason HA, Cronquist A (1991) Manual of vascular plants of northeastern United States and adjacent Canada. D. Van Nostrand Co. Inc., PrincetonCrossRefGoogle Scholar
  21. Greenleaf SS, Williams NM, Winfree R, Kremen C (2007) Bee foraging ranges and their relationship to body size. Oecologia 153:589–596CrossRefPubMedGoogle Scholar
  22. Gyan KY, Woodell SRJ (1987) Analysis of insect pollen loads and pollination efficiency of some common insect visitors of four species of woody Rosaceae. Funct Ecol 1:269–274CrossRefGoogle Scholar
  23. Hanley ME, Franco M, Pichon S, Darvill B, Goulson D (2008) Breeding system, pollinator choice and variation in pollen quality in British herbaceous plants. Funct Ecol 22:592–598CrossRefGoogle Scholar
  24. Hogendoorn K (1996) Socio-economics of brood destruction during supersedure in the carpenter bee Xylocopa pubescens. J Evol Biol 9:931–952CrossRefGoogle Scholar
  25. Hogendoorn K, Watiniasih NL, Schwarz MP (2001) Extended alloparental care in the almost solitary bee Exoneurella eremophila (Hymenoptera:Apidae). Behav Ecol Sociobiol 50:275–282CrossRefGoogle Scholar
  26. Human H, Nicolson SW, Strauss K, Pirk CWW, Dietemann V (2007) Influence of pollen quality on ovarian development in honeybee workers (Apis mellifera scutellata). J Insect Physiol 53:649–655CrossRefPubMedGoogle Scholar
  27. Hunt JH, Amdam GV (2005) Bivoltinism as an antecedent to eusociality in the paper wasp genus Polistes. Science 308:264–267CrossRefPubMedPubMedCentralGoogle Scholar
  28. Hunt JH, Nalepa CA (1994) Nourishment, evolution and insect sociality. In: Hunt JH, Nalepa CA (eds) Nourishment and evolution in insect societies. Westview Press, Oxford, pp. 1–19Google Scholar
  29. Johnson MD (1988) The relationship of provision weight to adult weight and sex ratio in the solitary bee, Ceratina calcarata. Ecol Entomol 13:165–170CrossRefGoogle Scholar
  30. Kapheim KM, Bernal SP, Smith AR, Nonacs P, Wcislo WT (2011) Support for maternal manipulation of developmental nutrition in a facultatively eusocial bee, Megalopta genalis (Halictidae). Behav Ecol Sociobiol 65:1179–1190CrossRefPubMedPubMedCentralGoogle Scholar
  31. Kapheim KM, Nonacs P, Smith AR, Wayne RK, Wcislo WT (2015) Kinship, parental manipulation and evolutionary origins of eusociality. Proc R Soc B 282:2014–2886CrossRefGoogle Scholar
  32. Kim JY (1999) Influence of resource level on maternal investment in a leaf-cutter bee (Hymenoptera:Megachilidae). Behav Ecol 10:552–556CrossRefGoogle Scholar
  33. Kobayashi-Kidokoro M, Higashi S (2010) Flower constancy in the generalist pollinator Ceratina flavipes (Hymenoptera:Apidae): an evaluation by pollen analysis. Psyche 2010:891906CrossRefGoogle Scholar
  34. Konzmann S, Lunau K (2014) Divergent rules for pollen and nectar foraging bumblebees—a laboratory study with artificial flowers offering diluted nectar substitute and pollen surrogate. PLoS One 9:e91900CrossRefPubMedPubMedCentralGoogle Scholar
  35. Li C, Xu B, Wang Y, Yang Z, Yang W (2014) Protein content in larval diet affects adult longevity and antioxidant gene expression in honey bee workers. Entomol Exp et Appl 151:19–26CrossRefGoogle Scholar
  36. Lin N, Michener CD (1972) Evolution of sociality in insects. Quart Rev Biol 47:1–159CrossRefGoogle Scholar
  37. Michener CD (1974) The social behavior of the bees: a comparative study. Harvard University Press, HarvardGoogle Scholar
  38. Michener CD (2007) The bees of the world. Johns Hopkins University Press, BaltimoreGoogle Scholar
  39. Michener CD, Brothers DJ (1974) Were workers of eusocial hymenoptera initially altruistic or oppressed. Proc Natl Acad Sci U S A 71:671–674CrossRefPubMedPubMedCentralGoogle Scholar
  40. Mousseau TA, Fox C (1998) Maternal effects as adaptations. Oxford University Press, New YorkGoogle Scholar
  41. Mueller UG (1991) Haplodiploidy and the evolution of facultative social sex ratios in a primitively eusocial bee. Science 254:442–444CrossRefPubMedGoogle Scholar
  42. Packer L, Knerer G (1985) Social evolution and its correlates in bees of the subgenus Evylaeus. Behav Ecol Sociobiol 17:143–149Google Scholar
  43. Pernal SF, Currie RW (2001) The influence of pollen quality on foraging behavior in honeybees (Apis mellifera). Behav Ecol Sociobiol 51:53–68CrossRefGoogle Scholar
  44. Queller DC (1996) The origin and maintenance of eusociality: the advantage of extended parental care. In: Turillazzi S, West-Eberhard MJ (eds) Natural history and evolution of paper-wasps. Oxford University Press, New York, pp. 218–234Google Scholar
  45. Quezada-Euan JJG, Lopez-Velasco A, Perez-Balam J, Moo-Valle H, Velazquez-Madrazo A, Paxton RJ (2010) Body size differs in workers produced across time and is associated with variation in the quantity and composition of larval food in Nannotrigona perilampoides (Hymenoptera, Meliponini). Insect Soc 58:31–38CrossRefGoogle Scholar
  46. Radmacher S, Strohm E (2010) Factors affecting offspring body size in the solitary bee Osmia bicornis (Hymenoptera, Megachilidae). Apidologie 41:169–177CrossRefGoogle Scholar
  47. Rayner CJ, Langridge DF (1985) Amino acids in bee-collected pollens from Australian indigenous and exotic plants. Aust J Exp Agric 25:722–726CrossRefGoogle Scholar
  48. Rehan SM, Richards MH (2010a) Nesting and life cycle of Ceratina calcarata in southern Ontario (Hymenoptera: Apidae:Xylocopinae). Can Entomol 142:65–74CrossRefGoogle Scholar
  49. Rehan SM, Richards MH (2010b) The influence of maternal quality on brood sex allocation in the small carpenter bee, Ceratina calcarata. Ethol 116:876–887Google Scholar
  50. Rehan SM, Richards MH (2013) Reproductive aggression and nestmate recognition in a subsocial bee. Anim Behav 85:733–741CrossRefGoogle Scholar
  51. Rehan SM, Toth AL (2015) Climbing the social ladder: molecular evolution of sociality. Trends Ecol Evol 30:426–433CrossRefPubMedGoogle Scholar
  52. Rehan SM, Leys R, Schwarz MP (2012) A mid-cretaceous origin of sociality in xylocopine bees with only two origins of true worker castes. PLoS One 7:e34690CrossRefPubMedPubMedCentralGoogle Scholar
  53. Rehan SM, Berens AJ, Toth AL (2014) At the brink of eusociality: transcriptomic correlates of worker behavior in a small carpenter bee. BMC Evol Biol 14:260CrossRefPubMedPubMedCentralGoogle Scholar
  54. Reinhold K (2002) Maternal effects and the evolution of behavioral and morphological characters: a literature review indicates the importance of extended maternal care. J Hered 93:400–405CrossRefPubMedGoogle Scholar
  55. Roulston TH, Cane JH (2000) Pollen nutritional content and digestibility for animals. Plant Syst Evol 222:187–209CrossRefGoogle Scholar
  56. Roulston TH, Cane JH (2002) The effect of pollen protein concentration on body size in the sweat bee Lasioglossum zephyrum (Hymenoptera:Apiformes). Evol Ecol 16:49–65CrossRefGoogle Scholar
  57. Roulston TH, Cane JH, Buchmann SL (2000) What governs protein content of pollen: pollinator preferences, pollen-pistil interaction, or phylogeny? Ecol Monogr 70:617–643Google Scholar
  58. Sakagami SF, Maeta Y (1977) Some presumably presocial habits of Japanese Ceratina bees, with notes on various social types in hymenoptera. Insect Soc 24:319–343CrossRefGoogle Scholar
  59. Sakagami SF, Maeta Y (1984) Multifemale nests and rudimentary castes in the normally solitary bee Ceratina japonica (Hymenoptera:Xylocopinae). J Kans Entomol Soc 57:639–656Google Scholar
  60. Sakagami SF, Maeta Y (1995) Task allocation in artificially induced colonies of a basically solitary bee Ceratina (Ceratinidia) okinawana, with a comparison of sociality between Ceratina and Xylocopa (Hymenoptera, Anthophoridae, Xylocopinae). Japanese J Ecol 63:115–150Google Scholar
  61. Shannon CE (1948) A mathematical theory of communication. Bell Syst Tech J 27:379–423CrossRefGoogle Scholar
  62. Shell WA, Rehan SM (2016) Recent and rapid diversification of the small carpenter bees in eastern North America. Biol J Linn Soc 117:633–645CrossRefGoogle Scholar
  63. Simpson EH (1949) Measurement of diversity. Nature 163:688CrossRefGoogle Scholar
  64. Smith AR, Quintero IJL, Patino JEM, Roubik DW, Wcislo WT (2012) Pollen use by Megalopta sweat bees in relation to resource availability in a tropical forest. Ecol Ento 37:309–317CrossRefGoogle Scholar
  65. Sokal RR, Rohlf FJ (1995) Biometry: the principles and practice of statistics in biological research, 4th edn. W. H. Freeman and Co, New YorkGoogle Scholar
  66. Somme L, Vanderplank M, Michez D, Lombaerdae I, Moerman R, Wathelet B, Wattiez R, Lognay G, Jacquemart AL (2014) Pollen and nectar quality drive the major and minor floral choices of bumble bees. Apidologie 46:92–106CrossRefGoogle Scholar
  67. Stacey PB, Koenig WD (1990) Cooperative breeding in birds: long-term studies of ecology and behavior. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  68. Sutcliffe GH, Plowright RC (1990) The effects of pollen availability on development time in the bumble bee Bombus terricola K. (Hymenoptera:Apidae). Can J Zool 68:1120–1123CrossRefGoogle Scholar
  69. Tasei J-N, Aupinel P (2008) Nutritive value of 15 single pollens and pollen mixes tested on larvae produced by bumblebee workers (Bombus terrestris, Hymenoptera:Apidae). Apidologie 39:397–409CrossRefGoogle Scholar
  70. Tepedino VJ, Torchio PF (1982) Temporal variability in sex ratio of a nonsocial bee, Osmia lignaria propinqua—extrinsic determination or tracking of an optimum. Oikos 38:177–182CrossRefGoogle Scholar
  71. Toth AL, Bilof KJ, Henshaw MT, Hunt JH, Robinson GE (2009) Lipid stores, ovary development, and gene expression in Polistes metricus females. Insect Soc 56:77–84CrossRefGoogle Scholar
  72. Vanderplanck M, Moerman R, Rasmont P, Lognay G, Wathelet B, Wattiez R, Michez D (2014) How does pollen chemistry impact development and feeding behaviour of polylectic bees? PLoS One 9:e86209CrossRefPubMedPubMedCentralGoogle Scholar
  73. Vaudo AD, Patch HM, Mortensen DA, Grozinger CM, Tooker JF (2014) Bumble bees exhibit daily behavioral patterns in pollen foraging. Arthropod-Plant Inter 8:273–283Google Scholar
  74. Vaudo AD, Tooker JF, Grozinger CM, Patch HM (2015) Bee nutrition and floral resource restoration. Curr Opin Insect Sci 10:133–141CrossRefGoogle Scholar
  75. Wade MJ (2001) Maternal effect genes and the evolution of sociality in haplo-diploid organisms. Evolution 55:453–458CrossRefPubMedGoogle Scholar
  76. West S (2009) Sex allocation. Princeton University Press, PrincetonCrossRefGoogle Scholar
  77. Westrich P (1996) Habitat requirements of central European bees and the problems of partial habitats. In: Matheson A, Buchmann SL, O’Toole C, Westrich P, Williams IH (eds) The conservation of bees. Academic Press, London, pp. 1–16Google Scholar
  78. Willard DA, Holmes CW, Korvela MS, Mason D, Murray JB, Orem WH, Towles DT (2003) Paleoecological insights on fixed tree island development in the Florida Everglades: I. Environmental controls. In: Sklar FH, van der Valk AG (eds) Tree islands of the Everglades. Kluwer Academic Publishers, Dordrecht, pp. 117–151Google Scholar
  79. Wilson AJ, Coltman DW, Pemberton JM, Overall ADJ, Byrne KA, Kruuk LEB (2005) Maternal genetic effects set the potential for evolution in a free-living vertebrate population. J Evol Biol 18:405–414CrossRefPubMedGoogle Scholar
  80. Wolf JB, Wade MJ (2009) What are maternal effects (and what are they not)? Phil Trans Roy Soc Lond B 364:1107–1115CrossRefGoogle Scholar
  81. Ziska LH, Pettis JS, Edwards J, Hancock JE, Tomecek MB, Clark A, Dukes JS, Loladze I, Polley HW (2016) Rising atmospheric CO2 is reducing the protein concentration of a floral pollen source essential for north American bees. Proc R Soc B 283:20160414CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Sarah P. Lawson
    • 1
  • Krista N. Ciaccio
    • 1
  • Sandra M. Rehan
    • 1
  1. 1.Department of Biological SciencesUniversity of New HampshireDurhamUSA

Personalised recommendations