Skip to main content
SpringerLink
Log in

Physiological plasticity of metabolic rates in the invasive honey bee and an endemic Australian bee species

  • Original Paper
  • Published:
Journal of Comparative Physiology B Aims and scope Submit manuscript

Abstract

Seasonal variation in metabolic rate and evaporative water loss as a function of ambient temperature were compared in two species of bees. The endemic blue-banded bee, Amegilla chlorocyanea, is a solitary species that is an important pollinator in the south-west Australian biodiversity hotspot. Responses were compared with the European honeybee, Apis mellifera, naturalised in Western Australia almost 200 years ago. Metabolic rate increased exponentially with temperature to a peak in both species, and then declined rapidly, with unique scaling exponents and peaks for all species-by-season comparisons. Early in the austral summer, Apis was less thermally tolerant than Amegilla, but the positions reversed later in the foraging season. There were also significant exponential increases in evaporative water loss with increasing temperature, and both season and species contributed to significantly different responses. Apis maintained relatively consistent thermal performance of metabolic rate between seasons, but at the expense of increased rates of evaporative water loss later in summer. In contrast, Amegilla had dramatically increased metabolic requirements later in summer, but maintained consistent thermal performance of evaporative water loss. Although both species acclimated to higher thermal tolerance, the physiological strategies underpinning the acclimation differed. These findings may have important implications for understanding the responses of these and other pollinators to changing environments and for their conservation management.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Abrol DP (2005) Pollination energetics. J Asia Pacific Entomol 8:3–14

    Article  Google Scholar 

  • Ahearn GA, Hadley NF (1969) The effects of temperature and humidity on water loss in two desert tenebrionid beetles, Eleodes armata and Cryptoglossa verrucosa. Comp Biochem Physiol 30:739–749

  • Aizen MA, Feinsinger P (1994) Forest fragmentation, pollination, and plant reproduction in a Chaco dry forest, Argentina. Ecology 75:330–351

    Article  Google Scholar 

  • Angilletta MJ (2006) Estimating and comparing thermal performance curves. J Therm Biol 31:541–545

    Article  Google Scholar 

  • Angilletta MJJ (2009) Thermal Adaptation: a Theoretical and empirical synthesis. Oxford University Press, Oxford

    Book  Google Scholar 

  • Baker HG (1965) Characteristics and modes of origin of weeds. In: Baker HG, Stebbins GL (eds) The Genetics of colonizing species. Academic Press, New York, pp 147–168

    Google Scholar 

  • Barton K (2013) MuMIn: multi-model inference version. R package version 1.9.13

  • Bates DM, Watts DG (1988) Nonlinear regression analysis and its applications. Wiley, New York

    Book  Google Scholar 

  • Berrigan D (1997) Acclimation of metabolic rate in response to developmental temperature in Drosophila melanogaster. J Therm Biol 22:213–218

    Article  Google Scholar 

  • Berrigan D, Partridge L (1997) Influence of temperature and activity on the metabolic rate of adult Drosophila melanogaster. Comp Biochem Physiol A 118:1301–1307

    Article  CAS  Google Scholar 

  • Booth DT, Kiddell K (2007) Temperature and the energetics of development in the house cricket (Acheta domesticus). J Insect Physiol 53:950–953

    Article  CAS  PubMed  Google Scholar 

  • Brodie RJ (2005) Desiccation resistance in megalopae of the terrestrial hermit crab Coenobita compressus: water loss and the role of the shell. Invertebr Biol 124:265–272

    Article  Google Scholar 

  • Brooks RW (1988) Systematics and phylogeny of the anthophorine bees (Hymenoptera: Anthophoridae; Anthophorini). University of Kansas Science Bulletin 53:436–575

    Google Scholar 

  • Buchmann SL (1983) Buzz pollination in angiosperms. In: Jones CE, Little RJ (eds) Handbook of experimental pollination biology. Van Nostrand-Rheinhold Inc, New York, pp 73–113

    Google Scholar 

  • Burnham KP, Anderson DR (2002) Model Selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer, New York

    Google Scholar 

  • Cardale J (1968) Nests and nesting behaviour of Amegilla (Amegilla) pulchra (Smith) (Hymenoptera: Apoidea: Anthophorinae). Aust J Zool 16:689–707

    Google Scholar 

  • Chown SL, Gaston KJ (2008) Macrophysiology for a changing world. Proc R Soc B 275:1469–1478

    Article  PubMed Central  PubMed  Google Scholar 

  • Chown SL, Nicholson SW (2004) Insect physiological ecology: mechanisms and patterns. Oxford University Press, Oxford

    Book  Google Scholar 

  • Chown SL, Pistorius PA, Scholtz CH (1998) Morphological correlates of flightlessness in southern African Scarabaeinae (Coleoptera: Scarabaeidae): testing a condition of the water conservation hypothesis. Can J Zool 76:1123–1133

    Article  Google Scholar 

  • Chown SL, Marais E, Terblanche JS, Klok CJ, Lighton JRB, Blackburn TM (2007) Scaling of insect metabolic rate is inconsistent with the nutrient supply network model. Funct Ecol 21:282–290

    Article  Google Scholar 

  • Cloudsley-Thompson JL (1991) Ecophysiology of desert arthropods and reptiles. Springer, Berlin

    Book  Google Scholar 

  • Dennis AJ, Green RJ, Schupp EW (2007) Seed dispersal: theory and its application in a changing world. CABI publishing, Wallingford

    Book  Google Scholar 

  • Dick CW, Etchelecu G, Austerlitz F (2003) Pollen dispersal of tropical trees (Dinizia excelsa: Fabaceae) by native insects and African honeybees in pristine and fragmented Amazonian rainforest. Mol Ecol 12:753–764

    Article  PubMed  Google Scholar 

  • Dixon KW (2009) Pollination and restoration. Science 325:571–573

    Article  CAS  PubMed  Google Scholar 

  • Dubitzky A (2007) Phylogeny of the world anthophorini (Hymenoptera: Apoidea: Apidae). Syst Entomol 32:585–600

    Article  Google Scholar 

  • Duncan DH, Cunningham SA, Nicotra AB (2004) High self-pollen transfer and low fruit set in buzz-pollinated Dianella revoluta (Phormiaceae). Aust J Bot 52:185–193

    Article  Google Scholar 

  • Dunstan H, Florentine SK, Calviño-Cancela M, Westbrooke ME, Palmer GC (2013) Dietary characteristics of Emus (Dromaius novaehollandiae) in semi-arid New South Wales, Australia, and dispersal and germination of ingested seeds. Emu 113:168–176

    Article  Google Scholar 

  • Edney EB (1977) Water balance in land arthropods. Springer, Berlin

    Book  Google Scholar 

  • Fahrenholz L, Lamprecht I, Schricker B (1989) Thermal investigations of a honey bee colony: thermoregulation of the hive during summer and winter and heat production of members of different bee castes. J Comp Physiol B 159:551–560

    Article  Google Scholar 

  • Feder ME (1987) The analysis of physiological diversity: the prospects for pattern documentation and general questions in ecological physiology. In: Feder ME, Bennett AF, Burggren WG, Huey RB (eds) New directions in ecological physiology. Cambridge University Press, Cambridge, pp 38–75

    Google Scholar 

  • Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1–15

    Article  Google Scholar 

  • Fewell JH, Winston ML (1992) Colony state and regulation of pollen foraging in the honey bee, Apis mellifera L. Behav Ecol Sociobiol 30:387–393

    Article  Google Scholar 

  • Fewell JH, Winston ML (1996) Regulation of nectar collection in relation to honey storage levels by honey bees, Apis mellifera. Behav Ecol 7:286–291

    Article  Google Scholar 

  • Fornberg B, Sloan DM (1994) A review of pseudospectral methods for solving partial differential equations. Acta Numerica 3:203–267

    Article  Google Scholar 

  • Garland TJ, Adolph SC (1994) Why not to do two-species comparative studies: limitations on inferring adaptation. Physiological Zoology 67:797–828

    Google Scholar 

  • Gilbert P, Varadhan R (2012) numDeriv: accurate numerical derivatives. R package version 2012.9-1

  • Glanville EJ, Seebacher F (2006) Compensation for environmental change by complementary shifts of thermal sensitivity and thermoregulatory behaviour in an ectotherm. J Exp Biol 209:4869–4877

    Article  CAS  PubMed  Google Scholar 

  • Gómez JM (2003) Spatial patterns in long-distance dispersal of Quercus ilex acorns by jays in a heterogeneous landscape. Ecography 26:573–584

    Article  Google Scholar 

  • Gross CL (2001) The effect of introduced honeybees on native bee visitation and fruit-set in Dillwynia juniperina (Fabaceae) in a fragmented ecosystem. Biol Conserv 102:89–95

    Article  Google Scholar 

  • Gross CL, Mackay D (1998) Honeybees reduce fitness in the pioneer shrub Melastoma affine (Melastomataceae). Biol Conserv 86:169–178

    Article  Google Scholar 

  • Gurka MJ, Edwards LJ (2011) Estimating variance components and random effects using the Box-Cox transformation in the linear mixed model. Commun Stat Theory Methods 40:515–531

    Article  Google Scholar 

  • Hadley NF (1994) Water relations of terrestrial arthropods. Academic Press, New York

  • Hayes JP, Shonkwiler JS (2006) Allometry, antilog transformations, and the perils of prediction on the original scale. Physiol Biochem Zool 79:665–674

    Article  PubMed  Google Scholar 

  • Hogendoorn K, Gross CL, Sedgley M, Keller MA (2006) Increased tomato yield through pollination by native Australian blue-banded bees (Amegilla chlorocyanea Cockerell). J Econ Entomol 99:828–833

    Article  PubMed  Google Scholar 

  • Hogendoorn K, Coventry SA, Keller MA (2007) Foraging behaviour of a blue banded bee, Amegilla (Notomegilla) chlorocyanea Cockerell in greenhouses: implications for use as tomato pollinators. Apidologie 38:86–92

    Article  Google Scholar 

  • Houston TF (2000) Native bees on wildflowers in western Australia. A synopsis of bee visitation of wildflowers based on the bee collection of the Western Australian Museum. Special Publication no. 2. Western Australian Insect Study Society, Perth

  • Houston TF, Ladd PG (2002) Buzz pollination in the Epacridaceae. Aust J Bot 50:83–91

    Article  Google Scholar 

  • Huey RB, Kingsolver JG (1989) Evolution of thermal sensitivity of ectotherm performance. Trends Ecol Evol 4:131–135

    Article  CAS  PubMed  Google Scholar 

  • Huey RB, Kingsolver JG (1993) Evolution of resistance to high temperature in ectotherms. Am Nat 142:S21–S46

    Article  Google Scholar 

  • Human H, Nicholson SW, Dietemann V (2006) Do honeybees, Apis mellifera scutellata, regulate humidity in their nest? Naturwissenschaften 93:397–401

    Article  CAS  PubMed  Google Scholar 

  • Kearns CA, Inouye DW, Waser NM (1998) Endangered mutualisms: the conservation of plant-pollinator interactions. Annu Rev Ecol Syst 29:83–112

    Article  Google Scholar 

  • Kevan PG, Tikhmenev EA, Usui M (1993) Insects and plants in the pollination ecology of the boreal zone. Ecol Res 8:247–267

    Article  Google Scholar 

  • Kovac H, Stabentheiner A, Hetz SK, Petz M, Crailsheim K (2007) Respiration of resting honeybees. J Insect Physiol 53:1250–1261

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kovac H, Käfer H, Stabentheiner A, Costa C (2014) Metabolism and upper thermal limits of Apis mellifera carnica and A. m. ligustica. Apidologie 45:664–677

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kronenberg F, Heller HC (1982) Colonial thermoregulation in Honey Bees (Apis mellifera). J Comp Physiol B 148:65–76

    Article  Google Scholar 

  • Lewontin RC (1969) The bases of conflict in biological explanation. J Hist Biol 2:35–53

    Article  Google Scholar 

  • Lighton JR, Lovegrove BG (1990) A temperature-induced switch from diffusive to convective ventilation in the Honeybee. J Exp Biol 154:509–516

    Google Scholar 

  • Machado IC, Lopes AV (2004) Floral traits and pollination systems in the Caatinga, a Brazilian tropical dry forest. Ann Bot 94:365–376

    Article  PubMed Central  PubMed  Google Scholar 

  • Martin TL, Huey RB (2008) Why “suboptimal” is optimal: Jensen’s inequality and ectotherm thermal preferences. Am Nat 171:E102–E118

    Article  PubMed  Google Scholar 

  • Mason LD, Tomlinson S, Withers PC, Main BY (2013) Thermal and hygric physiology of Australian burrowing mygalomorph spiders (Aganippe spp.). J Comp Physiol B 183:71–82

    Article  PubMed  Google Scholar 

  • Mazerolle MJ (2013) AICcmodavg: model selection and multimodel inference based on (Q)AIC(c). R package version 1:35

    Google Scholar 

  • McCallum KP, McDougall FO, Seymour RS (2013) A review of the energetics of pollination biology. J Comp Physiol B 183:867–876

    Article  PubMed  Google Scholar 

  • Mendes do Carmo R, Franceschinelli EV (2004) Introduced honeybees (Apis mellifera) reduce pollination success without affecting the floral resource taken by native pollinators. Biotropica 36:371–376

  • Menz MHM, Phillips RD, Winfree R, Kremen C, Aizen MA, Johnson SD, Dixon KW (2011) Reconnecting plants and pollinators: challenges in the restoration of pollination mutualisms. Trends Plant Sci 16:4–12

    Article  CAS  PubMed  Google Scholar 

  • Myers N, Mittermeier RA, Mittermeier CG, de Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858

    Article  CAS  PubMed  Google Scholar 

  • Nespolo RF, Bacigalupe LD, Rezende EL, Bozinovic F (2001) When nonshivering thermogenesis equals maximum metabolic rate: thermal acclimation and phenotypic plasticity of fossorial Spalacopus cyanus (Rodentia). Physiol Biochem Zool 74:325–332

    Article  CAS  PubMed  Google Scholar 

  • Paton DC (1993) Honeybees in the Australian environment—does Apis mellifera disrupt or benefit the native biota? Bioscience 43:95–101

    Article  Google Scholar 

  • Petanidou T, Vokou D (1990) Pollination and pollen energetics in Mediterranean ecosystems. Am J Bot 77:986–992

    Article  Google Scholar 

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

    Google Scholar 

  • Ritz C, Streibig JC (2008) Nonlinear regression with R. Springer, New York

    Google Scholar 

  • Sammataro D, Avitabile A (2011) The Beekeeper’s Handbook. Cornell University Press, New York

    Google Scholar 

  • Schmidt-Nielsen K (1983) Animal physiology : adaptation and environment. Cambridge University Press, New York

    Google Scholar 

  • Seebacher F (2005) A review of thermoregulation and physiological performance in reptiles: what is the role of phenotypic flexibility? J Comp Physiol B 175:453–461

    Article  PubMed  Google Scholar 

  • Seebacher F, Franklin CE (2012) Determining environmental causes of biological effects: the need for a mechanistic physiological dimension in conservation biology. Philos Trans R Soc Lond B 367:1607–1614

    Article  Google Scholar 

  • Seymour RS (1974) Convective and evaporative cooling in sawfly larvae. J Insect Physiol 20:2447–2457

    Article  CAS  PubMed  Google Scholar 

  • Smigel JT, Gibbs AG (2008) Conglobation in the pill bug, Armadillidium vulgare, as a water conservation mechanism. J Insect Sci 8:44

    Article  PubMed Central  Google Scholar 

  • Society for Ecological Restoration International Science and Policy Working Group (2004) SER international primer on ecological restoration. Society for Ecological Restoration, Washington, USA

    Google Scholar 

  • Strayer D (1999) Invasion of fresh waters by saltwater animals. Trends Ecol Evol 14:448–449

    Article  PubMed  Google Scholar 

  • Thurman CL (1998) Evaporative water loss, corporal temperature and the distribution of sympatric Fiddler Crabs (Uca) from South Texas. Comp Biochem Physiol 119A:279–286

    Article  CAS  Google Scholar 

  • Tomlinson S, Phillips RD (2012) Metabolic rate, evaporative water loss and field activity in response to temperature in an ichneumonid wasp. J Zool 287:81–90

    Article  Google Scholar 

  • Tomlinson S, Arnall S, Munn AJ, Bradshaw SD, Maloney SK, Dixon KW, Didham RK (2014) Applications and implications of ecological energetics. Trends Ecol Evol 29:280–290

    Article  PubMed  Google Scholar 

  • White CR, Portugal SJ, Martin GR, Butler PJ (2006) Respirometry: anhydrous Drierite equilibrates with carbon dioxide and increases washout times. Physiol Biochem Zool 79:977–980

    Article  PubMed  Google Scholar 

  • Whitfield CW, Behura SK, Berlocher SH, Clark AG, Johnston JS, Sheppard WS, Smith DR, Suarez AV, Weaver D, Tsutsui ND (2006) Thrice out of Africa: ancient and recent expansions of the honey bee, Apis mellifera. Science 314:642–645

    Article  CAS  PubMed  Google Scholar 

  • Winfree R, Gross BJ, Kremen C (2011) Valuing pollination services to agriculture. Ecol Econ 71:80–88

    Article  Google Scholar 

  • Withers PC (1992) Comparative Animal Physiology. Saunders College Publishing, Fort Worth

    Google Scholar 

  • Withers PC (2001) Design, calibration and calculation for flow-through respirometry systems. Aust J Zool 49:445–461

    Article  Google Scholar 

  • Wolff WJ (2000) Recent human-induced invasions of fresh waters by saltwater animals? Aquat Ecol 34:319–321

    Article  Google Scholar 

  • Wood SN (2008) Fast stable direct fitting and smoothness selection for generalized additive models. J R Stat Soc B 70:495–518

    Article  Google Scholar 

Download references

Acknowledgments

This research was funded under the Australian Research Council Linkage Grant LP110200304. Thanks go to Phillip Withers and Hai Ngo for the use of respirometry equipment and extensive technical advice. We also acknowledge the input of Tiffane Bates on good captive husbandry of Apis mellifera. Katja Hogendoorn is gratefully acknowledged for taxonomic advice on Amegilla. Carly Wilson was instrumental in capturing wild Amegilla chlorocyanea. Statistical advice was contributed by Christian Ritz and Michael Renton. Suggestions made by two anonymous peer reviewers strengthened and improved the manuscript substantially.

Author information

Authors and Affiliations

  1. School of Animal Biology, The University of Western Australia, 35 Stirling Highway, Crawley, WA, 6009, Australia

    Sean Tomlinson, Raphael K. Didham & S. Don Bradshaw

  2. Kings Park and Botanic Gardens, The Botanic Gardens and Parks Authority, Fraser Avenue, West Perth, WA, 6005, Australia

    Sean Tomlinson

  3. Department of Environment and Agriculture, Curtin University, Kent Street, Bentley, WA, 6102, Australia

    Kingsley W. Dixon

  4. School of Plant Biology, The University of Western Australia, Nedlands, WA, 6009, Australia

    Kingsley W. Dixon

  5. CSIRO Land & Water, Centre for Environment and Life Sciences, Underwood Ave, Floreat, WA, 6014, Australia

    Raphael K. Didham

Authors
  1. Sean Tomlinson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kingsley W. Dixon
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Raphael K. Didham
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. S. Don Bradshaw
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sean Tomlinson.

Additional information

Communicated by I.D. Hume.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 12 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tomlinson, S., Dixon, K.W., Didham, R.K. et al. Physiological plasticity of metabolic rates in the invasive honey bee and an endemic Australian bee species. J Comp Physiol B 185, 835–844 (2015). https://doi.org/10.1007/s00360-015-0930-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00360-015-0930-8

Keywords

Search

Navigation