Skip to main content
Log in

Measurement of protein and sugar consumed by bumblebee larvae under standard and food stress conditions using lanthanide complexes

  • Research Article
  • Published:
Insectes Sociaux Aims and scope Submit manuscript

Abstract

Measurement of food consumed by larvae of progressive provisioning bees requires an experimental approach that marks the food sources appropriately. This paper aims to measure the amount of sugars and proteins consumed by a single bumblebee larva and to define, how the proportion between protein and sugar changes under stress conditions. We marked sugar and pollen sources using lanthanide (gadolinium, dysprosium) complexes with diethylene-triamine-pentaacetic acid (DTPA) chelator. We precisely quantified the amount of Gd and Dy in feces, and thus quantified linearly correlated protein and sugar consumed by males and females (workers) of Bombus terrestris during their development. We compared body mass, total amount of ingested sugar and total amount of ingested protein in colonies which are fed ad libitum and in colonies with restricted feeding. Males fed ad libitum during their development ingested 0.52 mg of protein and 4.43 mg of sugar, and workers fed ad libitum ingested 0.54 mg of protein and 4.26 mg of sugar per 1 mg of dry body weight on average. Food-stressed workers ingested 0.51 mg of protein and 4.65 mg of sugar per 1 mg of dry body weight on average. Strong positive correlation between body mass, total protein ingested, and total sugar ingested in all our experiments was present. However, the consumption of sugar grew steeper with the consumption of protein in colonies under food stress compared to the ad libitum-fed colonies. In conclusion, we show the existence of different patterns in ingestion of protein and sugar between well-fed and food-stressed bumblebee colonies.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Alcock J, Simmons LW, Beveridge M (2005) Seasonal change in offspring sex and size in Dawson’s burrowing bees (Amegilla dawsoni) (Hymenoptera: Anthophorini). Ecol Entomol 30:247–254

    Article  Google Scholar 

  • Alford DV (1975) Bumblebees. Davis-Poynter, London

    Google Scholar 

  • Alexander RD (1974) The evolution of social behavior. Annu Rev Ecol Syst 5:325–383

    Article  Google Scholar 

  • Anon (1997) Aplikační list č. 46 [Dionex Application Sheet No. 46]. Dionex Corporation, Sunnyvale

    Google Scholar 

  • Ashford DA, Smith WA, Douglas AE (2000) Living on a high sugar diet: the fate of sucrose ingested by a phloem-feeding insect, the pea aphid Acyrthosiphon pisum. J Insect Physiol 46:335–341

    Article  CAS  PubMed  Google Scholar 

  • Aupinel P, Fortini D, Dufour H, Taséi JN, Michaud B, Odoux J-F, Pham-Delègue MH (2005) Improvement of artificial feeding in a standard in vitro method for rearing Apis mellifera larvae. Bull Insect 58:107–111

    Google Scholar 

  • Bishop GH (1961) Growth rates of honey bee larva. J Exp Zool A Ecol Genet Physiol 146:11–20

    Google Scholar 

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

    Article  Google Scholar 

  • Brand N, Chapuisat M (2012) Born to be bee, fed to be worker? The caste system of a primitively eusocial insect. Front Zool 9:35

    Article  PubMed  PubMed Central  Google Scholar 

  • Brodschneider R, Crailsheim K (2010) Nutrition and health in honey bees. Apidologie 41:278–294

    Article  Google Scholar 

  • Corbet SA (2003) Nectar sugar content: estimating standing crop and secretion rate in the field. Apidologie 34:1–10

    Article  CAS  Google Scholar 

  • Couvillon MJ, Dornhaus A (2010) Small worker bumble bees (Bombus impatiens) are hardier against starvation than their larger sisters. Insect Soc 57:193–197

    Article  CAS  Google Scholar 

  • Czekońska K, Chuda-Mickiewicz B, Samborski J (2015) Quality of honeybee drones reared in colonies with limited and unlimited access to pollen. Apidologie 46:1–9

    Article  Google Scholar 

  • Haydak MH (1970) Honey bee nutrition. Annu Rev Entomol 15:143–156

    Article  Google Scholar 

  • Heinrich B (1979) Bumblebee economics. Harvard University Press, Cambridge Massachusetts

    Google Scholar 

  • Hrassnigg N, Crailsheim K (2005) Differences in drone and worker physiology in honeybees (Apis mellifera). Apidologie 36:255–277

    Article  Google Scholar 

  • Jay SC (1963) The development of Honeybees in their cells. J Apicult Res 2:117–134

    Article  Google Scholar 

  • Johnson MD (1988) The relationship of provision weight to adult weight and sex-ratio in the solitary bee, Ceratina calcarata. Ecol Entomol 13:165–170

    Article  Google Scholar 

  • Kaftanoglu O, Linksvayer TA, Page RE (2011) Rearing honey bees, Apis mellifera, in vitro I: effects of sugar concentrations on survival and development. J Insect Sci 11:1–10

    Article  Google Scholar 

  • 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 65:1179–1190

    Article  PubMed  PubMed Central  Google Scholar 

  • Kim J (1999) Influence of resource level on maternal investment in a leaf-cutter bee (Hymenoptera: Megachilidae). Behav Ecol 10:552–556

    Article  Google Scholar 

  • Lawson SP, Ciaccio KN, Rehan SM (2016) Maternal manipulation of pollen provisions affects worker production in a small carpenter bee. Behav Ecol Sociobiol 70:1891–1900

    Article  Google Scholar 

  • Merbach A, Helm L, Tóth É (2013) The chemistry of contrast agents in medical magnetic resonance imaging. Wiley, Chichester

    Book  Google Scholar 

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

    Google Scholar 

  • Michener CD (2007) The bees of the world, 2nd edn. The Johns Hopkins University Press, Baltimore

    Google Scholar 

  • Moerman R, Vanderplanck M, Roger N, Declèves S, Wathelet B, Rasmont P, Fournier D, Michez D (2016) Growth rate of bumblebee larvae is related to pollen amino acids. J Econ Entomol 109:25–30

    Article  CAS  PubMed  Google Scholar 

  • Moerman R, Vanderplanck M, Fournier D, Jacquemart AL, Michez D (2017) Pollen nutrients better explain bumblebee colony development than pollen diversity. Insect Conserv Divers 10:171–179

    Article  Google Scholar 

  • Nelson JA, Sturtevant AP, Lineburg B (1924) Growth and feeding of honeybee larvae. United States Depart Agric, Depart Bull 1222:1–37

    Google Scholar 

  • Nicolson SW (2011) Bee food: the chemistry and nutritional value of nectar, pollen and mixtures of the two. Afr Zool 46:197–204

    Article  Google Scholar 

  • Nixon HL, Ribbands CR (1952) Food Transmission within the Honeybee Community. Proc R Soc Lond B Biol Sci 140:43–50

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Peterson JH, Roitberg BD (2016) Variable flight distance to resources results in changing sex allocation decisions, Megachile rotundata. Behav Ecol Sociobiol 70:247–253

    Article  Google Scholar 

  • Peterson JH, Roitberg BD (2006) Impacts of flight distance on sex ratio and resource allocation to offspring in the leafcutter bee, Megachile rotundata. Behav Ecol Sociobiol 59:589–596

    Article  Google Scholar 

  • Plowright R, Pendrel B (1977) Larval growth in bumble bees (Hymenoptera: Apidae). Can Entomol 109:967–973

    Article  Google Scholar 

  • Plowright RC, Thomson JD, Lefkovitch LP, Plowright CMS (1993) An experimental study of the effect of colony resource level manipulation on foraging for pollen by worker bumble bees (Hymenoptera: Apidae). Can J Zool 71:1393–1396

    Article  Google Scholar 

  • Quezada-Euán J, López-Velasco A, Pérez-Balam J, Moo-Valle H, Velazquez-Madrazo A, Paxton R (2011) 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 58:31–38

    Article  Google Scholar 

  • R Core Team (2014) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Rabie AL, Wells JD, Dent LK (1983) The nitrogen content of pollen protein. J Apicult Res 22:119–123

    Article  CAS  Google Scholar 

  • Radmacher S, Strohm E (2010) Factors affecting offspring body size in the solitary bee Osmia bicornis (Hymenoptera, Megachilidae). Apidologie 41:169–177

    Article  Google Scholar 

  • Řehoř I, Macháčková L, Bučánková A, Matějková S, Černá K, Straka J (2014) Measuring the sugar consumption of larvae in bumblebee micro-colonies: a promising new method for tracking food economics in bees. Apidologie 45:116–128

    Article  CAS  Google Scholar 

  • Ribeiro M, Velthuis HHW, Duchateau MJ (1993) Growth in bumblebee larvae: relations between the age of the larvae, their weight and the amount of pollen ingested by them. Proc Sect Exper Appl Entomol 4:121–125

    Google Scholar 

  • Ribeiro MF, Velthuis HHW, Duchateau MJ, van der Tweel I (1999) Feeding frequency and caste differentiation in Bombus terrestris larvae. Insectes Soc 46:306–314

    Article  Google Scholar 

  • Rortais A, Arnold G, Halm MP, Touffet-Briens F (2005) Modes of honeybees exposure to systemic insecticides: estimated amounts of contaminated pollen and nectar consumed by different categories of bees. Apidologie 36:71–83

    Article  CAS  Google Scholar 

  • Roger N, Michez D, Wattiez R, Sheridan C, Vanderplanck M (2017) Diet effects on bumblebee health. J Insect Physiol 96:128–133

    Article  CAS  PubMed  Google Scholar 

  • Rosenheim JA, Nonacs P, Mangel M (1996) Sex ratios and multifaceted parental investment. Am Nat 148:501–535

    Article  Google Scholar 

  • Roulston TH, Cane JH (2000) Pollen nutritional content and digestibility for animals. Plant Syst Evol 222:187–209

    Article  CAS  Google Scholar 

  • Roulston TH, Cane JH (2002) The effect of pollen protein concentration on body size in the sweat bee Lasioglossum zephyrum (Hymenoptera: Apiformes). Evol Ecol 16:49–65

    Article  Google Scholar 

  • Roulston TH, Cane JH, Buchmann SL (2000) What governs protein content of pollen: pollinator preferences, pollen–pistil interactions, or phylogeny? Ecol Monog 70:617–643

    Google Scholar 

  • Ruedenauer FA, Spaethe J, Leonhardt SD (2015) How to know which food is good for you: bumblebees use taste to discriminate between different concentrations of food differing in nutrient content. J Exp Biol 218:2233–2240

    Article  PubMed  Google Scholar 

  • Smeets PAM, Duchateau MJ (2001) Feeding behaviour in the bumble bee Bombus terrestris. Belg J Zool 131(Supplement 2):119–126

    Google Scholar 

  • Strohm E, Linsenmair KE (1997) Low resource availability causes extremely male-biased investment ratios in the European beewolf, Philanthus triangulum F. (Hymenoptera, Sphecidae). Proc R Soc Lond B Biol Sci 264:423–429

    Article  Google Scholar 

  • Sutcliffe G, Plowright R (1988) The effects of food supply on adult size in the bumblebee Bombus terricola Kirby (Hymenoptera: Apidae). Canad Entomol 120:1051–1058

    Article  Google Scholar 

  • 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 68:1120–1123

    Article  Google Scholar 

  • Tasei JN, Aupinel P (2008) Nutritive value of 15 single pollens and pollen mixes tested on larvae produced by bumblebee workers (Bombus terrestris, Hymenoptera: Apidae). Apidologie 39:397–409

    Article  CAS  Google Scholar 

  • 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:e86209

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Waldbauer GP (1968) The consumption and utilization of food by insects. In: Beament JWL, Treherne JE, Wigglesworth VB (eds) Advances in insect physiology. Academic Press, London, pp 229–288

    Google Scholar 

Download references

Acknowledgements

We would like to thank Vojtěch Kubíček (Department of Inorganic Chemistry, Faculty of Science, Charles University) for help with the preparation of lanthanide complexes. We thank Tereza Fraňková for language proofreading of the text. The study was supported by the Grant Agency of Charles University (project no. 338815/2015) (to LM), the SVV (Specific University Research) project no. 260434/2018 (to LM, MM and JS); the Ministry of Culture of the Czech Republic (DKRVO 2018/13, National Museum, Prague, 00023272) (to LM); the framework of the Czech National Agency for Agriculture Research by the Ministry of Agriculture of the Czech Republic (Earth QK 1810233) and institutional support from the Ministry of Agriculture of the Czech Republic (MZE-RO1718) (to AV).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to J. Straka.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Macháčková, L., Votavová, A., Mikát, M. et al. Measurement of protein and sugar consumed by bumblebee larvae under standard and food stress conditions using lanthanide complexes. Insect. Soc. 66, 245–256 (2019). https://doi.org/10.1007/s00040-018-00681-w

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00040-018-00681-w

Keywords

Navigation