Skip to main content

Indicators of Pollinator Decline and Pollen Limitation

  • Chapter
  • First Online:
Environmental Indicators

Abstract

Pollination is a crucial process for maintaining plant reproduction, and is responsible to the yield of about two third of the world’s crops. In recent years, there are growing concerns over pollinator declines and global pollination crisis. A decrease in pollinator populations also affects plants’ reproductive success, and alters the composition of wild plant communities. The main drivers for pollination decline are agriculture intensification and the subsequent fragmentation and loss of habitats, as well as introduction of non-native species and indirect effects of global climate change. Specialist pollinators and self-incompatible plants are seemingly in higher vulnerability. Our current knowledge of environmental effects on pollination processes is limited by the relatively little knowledge of the ecological requirements of pollinators and plants, and by the shortage of studies on the response of populations and communities to changes in land use. In this chapter we provide indices for estimating pollinator decline in both local and landscape scale, and discuss the relative efficiency of taxonomic and environmental indicators and indicators for estimating pollination services. We propose that future research should include developing and testing cost-effectiveness of indicators for patterns of pollinators’ diversity and of indicators for pollination services. These indicators should be tested in various ecological and spatial scales.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Aguilar R, Ashworth L, Galetto L, Aizen MA (2006) Plant reproductive susceptibility to habitat fragmentation: review and synthesis through a meta-analysis. Ecol Lett 9:968–980

    Article  Google Scholar 

  • Aizen MA, Harder LD (2007) Expanding the limits of the pollen-limitation concept: effects of pollen quantity and quality. Ecology 88:271–281

    Article  Google Scholar 

  • Aizen MA, Harder LD (2009) The Global stock of domesticated honey bees is growing slower than agricultural demand for pollination. Curr Biol 19:915–918

    Article  CAS  Google Scholar 

  • Aizen MA, Morales CL, Morales JM (2008) Invasive mutualists erode native pollination webs. PLoS Biol 6:e31

    Article  Google Scholar 

  • Ashman T-L et al (2004) Pollen limitation of plant reproduction: ecological and evolutionary causes and consequences. Ecology 85:2408–2421

    Article  Google Scholar 

  • Bartomeus I, Vila M, Santamaria L (2008) Contrasting effects of invasive plants in plant-pollinator networks. Oecologia 155:761–770

    Article  Google Scholar 

  • Bartomeus I et al (2013) Historical changes in northeastern US bee pollinators related to shared ecological traits. Proc Natl Acad Sci U S A 110:4656–4660

    Article  CAS  Google Scholar 

  • Biesmeijer JC et al (2006) Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 313:351–354

    Article  CAS  Google Scholar 

  • Brittain CA, Vighi M, Bommarco R, Settele J, Potts SG (2010) Impacts of a pesticide on pollinator species richness at different spatial scales. Basic Appl Ecol 11:106–115

    Article  CAS  Google Scholar 

  • Burd M (1994) Bateman’s principle and plant reproduction: the role of pollen limitation in fruit and seed set. Bot Rev 60:83–139

    Article  Google Scholar 

  • Burkle LA, Marlin JC, Knight TM (2013) Plant-pollinator interactions over 120 years: loss of species, co-occurrence, and function. Science 339:1611–1615

    Article  CAS  Google Scholar 

  • Calinger KM, Queenborough S, Curtis PS (2013) Herbarium specimens reveal the footprint of climate change on flowering trends across north-central North America. Ecol Lett 16:1037–1044

    Article  Google Scholar 

  • Cameron SA et al (2011) Patterns of widespread decline in North American bumble bees. Proc Natl Acad Sci U S A 108:662–667

    Article  CAS  Google Scholar 

  • Campbell LG, Husband BC (2007) Small populations are mate-poor but pollinator-rich in a rare, self-incompatible plant, Hymenoxys herbacea (Asteraceae). New Phytol 174:915–925

    Article  CAS  Google Scholar 

  • Carré G et al (2009) Landscape context and habitat type as drivers of bee diversity in European annual crops. Agric Ecosyst Environ 133:40–47

    Article  Google Scholar 

  • Chen IC, Hill JK, Ohlemuller R, Roy DB, Thomas CD (2011) Rapid range shifts of species associated with high levels of climate warming. Science 333:1024–1026

    Article  CAS  Google Scholar 

  • Christian CE (2001) Consequences of a biological invasion reveal the importance of mutualism for plant communities. Nature 413:635–639

    Article  CAS  Google Scholar 

  • Colla SR, Packer L (2008) Evidence for decline in eastern North American bumblebees (Hymenoptera: Apidae), with special focus on Bombus affinis Cresson. Biodivers Conserv 17:1379–1391

    Article  Google Scholar 

  • Conner JK, Davis R, Rush S (1995) The effect of wild radish floral morphology on pollination efficiency by four taxa of pollinators. Oecologia 104:234–245

    Article  Google Scholar 

  • Cunningham SA (2000) Depressed pollination in habitat fragments causes low fruit set. Proc Roy Soc Lond B Biol 267:1149–1152

    Article  CAS  Google Scholar 

  • Dafni A, Kevan PG, Husband BC (eds) (2005) Practical pollination biology. Enviroquest, Cambridge

    Google Scholar 

  • Delaplane KS, Mayer DF (2000) Crop pollination by bees. CABI Publishing, Wallingford

    Book  Google Scholar 

  • Fishman MA, Hadany L (2013) Pollinators’ mating rendezvous and the evolution of floral advertisement. J Theor Biol 316:99–106

    Article  Google Scholar 

  • Forister ML et al (2010) Compounded effects of climate change and habitat alteration shift patterns of butterfly diversity. Proc Natl Acad Sci U S A 107:2088–2092

    Article  CAS  Google Scholar 

  • Forrest JRK, Thomson JD (2011) An examination of synchrony between insect emergence and flowering in Rocky Mountain meadows. Ecol Monogr 81:469–491

    Article  Google Scholar 

  • Genersch E (2010) Honey bee pathology: current threats to honey bees and beekeeping. Appl Microbiol Biotechnol 87:87–97

    Article  CAS  Google Scholar 

  • Gonzalez-Varo JP, Traveset A (2010) Among-individual variation in pollen limitation and inbreeding depression in a mixed-mating shrub. Ann Bot-Lond 106:999–1008

    Article  Google Scholar 

  • González-Varo JP, Arroyo J, Aparicio A (2009) Effects of fragmentation on pollinator assemblage, pollen limitation and seed production of Mediterranean myrtle (Myrtus communis). Biol Conserv 142:1058–1065

    Article  Google Scholar 

  • González-Varo JP et al (2013) Combined effects of global change pressures on animal-mediated pollination. Trends Ecol Evol 28:524–530

    Article  Google Scholar 

  • Gotlieb A, Hollender Y, Mandelik Y (2011) Gardening in the desert changes bee communities and pollination network characteristics. Basic Appl Ecol 12:310–320

    Article  Google Scholar 

  • Goulson D, Hanley ME, Darvill B, Ellis JS (2006) Biotope associations and the decline of bumblebees (Bombus spp.). J Insect Conserv 10:95–103

    Article  Google Scholar 

  • Grundel R, Jean RP, Frohnapple KJ, Glowacki GA, Scott PE, Pavlovic NB (2010) Floral and nesting resources, habitat structure, and fire influence bee distribution across an open-forest gradient. Ecol Appl 20:1678–1692

    Article  Google Scholar 

  • Hinners SJ, Kearns CA, Wessman CA (2012) Roles of scale, matrix, and native habitat in supporting a diverse suburban pollinator assemblage. Ecol Appl 22:1923–1935

    Article  Google Scholar 

  • Holzschuh A, Steffan-Dewenter I, Kleijn D, Tscharntke T (2007) Diversity of flower-visiting bees in cereal fields: effects of farming system, landscape composition and regional context. J Appl Ecol 44:41–49

    Article  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 

  • Klank C, Pluess AR, Ghazoul J (2010) Effects of population size on plant reproduction and pollinator abundance in a specialized pollination system. J Ecol 98:1389–1397

    Article  Google Scholar 

  • Klein A-M et al (2007) Importance of pollinators in changing landscapes for world crops. Proc Roy Soc Lond B Biol 274:303–313

    Article  Google Scholar 

  • Knight TM et al (2005) Pollen limitation of plant reproduction: pattern and process. Ann Rev Ecol Evol Syst 36:467–497

    Article  Google Scholar 

  • Larson BMH, Barrett SCH (2000) A comparative analysis of pollen limitation in flowering plants. Biol J Linn Soc 69:503–520

    Article  Google Scholar 

  • Lonsdorf E, Kremen C, Ricketts T, Winfree R, Williams N, Greenleaf S (2009) Modelling pollination services across agricultural landscapes. Ann Bot-Lond 103:1589–1600

    Article  Google Scholar 

  • Lopes L, Buzato S (2007) Variation in pollinator assemblages in a fragmented landscape and its effects on reproductive stages of a self-incompatible treelet, Psychotria suterella (Rubiaceae). Oecologia 154:305–314

    Article  Google Scholar 

  • Mandelik Y, Roll U, Fleischer A (2010) Cost-efficiency of biodiversity indicators for Mediterranean ecosystems and the effects of socio-economic factors. J Appl Ecol 47:1179–1188

    Article  Google Scholar 

  • Mandelik Y, Dayan T, Chikatunov V, Kravchenko V (2012a) The relative performance of taxonomic vs. environmental indicators for local biodiversity assessment: a comparative study. Ecol Indic 15:171–180

    Article  Google Scholar 

  • Mandelik Y, Winfree R, Neeson T, Kremen C (2012b) Complementary habitat use by wild bees in agro-natural landscapes. Ecol Appl 22:1535–1546

    Article  Google Scholar 

  • Minckley RL, Roulston TH (2006) Incidental mutualisms and pollen specialization among bees. In: Waser NM, Ollerton J (eds) Plant-pollinator interactions: from specialization to generalization. The University of Chicago Press, Chicago, pp 69–99

    Google Scholar 

  • Müller A (2013) Palaearctic osmiine bees. ETH, Zürich

    Google Scholar 

  • Murray TE, Fitzpatrick U, Byrne A, Fealy R, Brown MJF, Paxton RJ (2012) Local-scale factors structure wild bee communities in protected areas. J Appl Ecol 49:998–1008

    Article  Google Scholar 

  • National Research Council (2007) Status of pollinators in North America. National Academies Press, Washington, DC

    Google Scholar 

  • Ne’eman G, Jurgens A, Newstrom-Lloyd L, Potts SG, Dafni A (2010) A framework for comparing pollinator performance: effectiveness and efficiency. Biol Rev 85:435–451

    Google Scholar 

  • Neeson TM, Van Rijn I, Mandelik Y (2013) How taxonomic diversity, community structure, and sample size determine the reliability of higher taxon surrogates. Ecol Appl 23:1216–1225

    Article  Google Scholar 

  • Ollerton J, Winfree R, Tarrant S (2011) How many flowering plants are pollinated by animals? Oikos 120:321–326

    Article  Google Scholar 

  • Ovaskainen O et al (2013) Community-level phenological response to climate change. Proc Natl Acad Sci U S A 110:13434–13439

    Article  CAS  Google Scholar 

  • Paini DR (2004) Impact of the introduced honey bee (Apis mellifera) (Hymenoptera: Apidae) on native bees: a review. Austral Ecol 29:399–407

    Article  Google Scholar 

  • Pauw A (2007) Collapse of a pollination web in small conservation areas. Ecology 88:1759–1769

    Article  Google Scholar 

  • Pauw A, Hawkins JA (2011) Reconstruction of historical pollination rates reveals linked declines of pollinators and plants. Oikos 120:344–349

    Article  Google Scholar 

  • Persson AS, Smith HG (2013) Seasonal persistence of bumblebee populations is affected by landscape context. Agric Ecosyst Environ 165:201–209

    Article  Google Scholar 

  • Potts SG et al (2003) Response of plant-pollinator communities to fire: changes in diversity, abundance and floral reward structure. Oikos 101:103–112

    Article  Google Scholar 

  • Potts SG et al (2005) Role of nesting resources in organising diverse bee communities in a Mediterranean landscape. Ecol Entomol 30:78–85

    Article  Google Scholar 

  • Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE (2010a) Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol 25:345–353

    Article  Google Scholar 

  • Potts SG et al (2010b) Declines of managed honey bees and beekeepers in Europe. J Apic Res 49:15–22

    Article  Google Scholar 

  • Proctor M, Yeo P, Lack A (1996) The natural history of pollination. Harper Collins, London

    Google Scholar 

  • Rafferty NE, Ives AR (2012) Pollinator effectiveness varies with experimental shifts in flowering time. Ecology 93:803–814

    Article  Google Scholar 

  • Rodrigues ASL, Brooks TM (2007) Shortcuts for biodiversity conservation planning: the effectiveness of surrogates. In: Annual review of ecology, evolution, and systematics, vol 38. Annual Reviews, Palo Alto, pp 713–737

    Google Scholar 

  • Sapir Y, Mazzucco R (2012) Post-zygotic reproductive isolation among populations of Iris atropurpurea: the effect of spatial distance among crosses and the role of inbreeding and outbreeding depression in determining niche width. Evol Ecol Res 14:425–445

    Google Scholar 

  • Sapir Y, Shmida A, Ne’eman G (2005) Pollination of the Oncocyclus irises (Iris: Iridaceae) by night-sheltering male bees. Plant Biol 7:417–424

    Article  CAS  Google Scholar 

  • Schiestl FP (2005) On the success of a swindle: pollination by deception in orchids. Naturwissenschaften 92:255–264

    Article  CAS  Google Scholar 

  • Segal B, Sapir Y, Carmel Y (2007) Fragmentation and pollination crisis in the self-incompatible Iris bismarckiana (Iridaceae), with implications for conservation. Isr J Ecol Evol 52:111–122

    Article  Google Scholar 

  • Sheffield CS, Kevan PG, Pindar A, Packer L (2013a) Bee (Hymenoptera: Apoidea) diversity within apple orchards and old fields in the Annapolis Valley, Nova Scotia, Canada. Can Entomol 145:94–114

    Article  Google Scholar 

  • Sheffield CS, Pindar A, Packer L, Kevan PG (2013b) The potential of cleptoparasitic bees as indicator taxa for assessing bee communities. Apidologie 44:501–510

    Article  Google Scholar 

  • Sjödin NE, Bengtsson J, Ekbom B (2008) The influence of grazing intensity and landscape composition on the diversity and abundance of flower-visiting insects. J Appl Ecol 45:763–772

    Article  Google Scholar 

  • Steffan-Dewenter I, Potts SG, Packer L (2005) Pollinator diversity and crop pollination services are at risk. Trends Ecol Evol 20:651–652

    Article  Google Scholar 

  • Temeles EJ, Kress WJ (2003) Adaptation in a plant-hummingbird association. Science 300:630–633

    Article  CAS  Google Scholar 

  • Thomson D (2004) Competitive interactions between the invasive European honey bee and native bumble bees. Ecology 85:458–470

    Article  Google Scholar 

  • Van Rijn I (2012) Evaluation of factors affecting the performance of the ‘Higher Taxa Approach’ (HTA) for assessing richness and composition in bee communities. In, vol. Master. The Hebrew University of Jerusalem, Rehovot

    Google Scholar 

  • Watts S, Sapir Y, Segal B, Dafni A (2013) The endangered Iris atropurpurea (Iridaceae) in Israel: honey-bees, night-sheltering male bees and female solitary bees as pollinators. Ann Bot 111:395–407

    Article  Google Scholar 

  • Wcislo WT, Cane JH (1996) Floral resource utilization by solitary bees (Hymenoptera: Apoidea) and exploitation of their stored foods by natural enemies. Ann Rev Entomol 41:257–286

    Article  CAS  Google Scholar 

  • Williams P, Colla S, Xie ZH (2009) Bumblebee vulnerability: common correlates of winners and losers across three continents. Conserv Biol 23:931–940

    Article  Google Scholar 

  • Willmer P (2011) Pollination and floral ecology. Princeton University Press, Princeton

    Book  Google Scholar 

  • Winfree R, Williams NM, Dushoff J, Kremen C (2007) Native bees provide insurance against ongoing honey bee losses. Ecol Lett 10:1105–1113

    Article  Google Scholar 

  • Winfree R, Aguilar R, Vazquez DP, LeBuhn G, Aizen MA (2009) A meta-analysis of bees’ responses to anthropogenic disturbance. Ecology 90:2068–2076

    Article  Google Scholar 

  • Winter C, Lehmann S, Diekmann M (2008) Determinants of reproductive success: a comparative study of five endangered river corridor plants in fragmented habitats. Biol Conserv 141:1095–1104

    Article  Google Scholar 

  • Yoshihara Y, Chimeddorj B, Buuueibaatar B, Lhaquasuren B, Takatsuki S (2008) Effects of livestock grazing on pollination on a steppe in eastern Mongolia. Biol Conserv 141:2376–2386

    Article  Google Scholar 

Download references

Acknowledgements

We thank Robert Armon and Osmo Hänninen for the invitation to write this chapter. Studies related to this chapter were supported by the Israel Science Foundation (YS and AD, YM), the Nekudat Hen program for promoting agricultural – Ecological projects (YS and AD, YM), and Porter School for Environmental Studies at Tel Aviv University (YS).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yuval Sapir .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2015 Springer Science+Business Media Dordrecht

About this chapter

Cite this chapter

Sapir, Y., Dorchin, A., Mandelik, Y. (2015). Indicators of Pollinator Decline and Pollen Limitation. In: Armon, R., Hänninen, O. (eds) Environmental Indicators. Springer, Dordrecht. https://doi.org/10.1007/978-94-017-9499-2_8

Download citation

Publish with us

Policies and ethics