Skip to main content
Log in

Nectar thieves or invited pollinators? A case study of tansy flowers and common house mosquitoes

  • Original Paper
  • Published:
Arthropod-Plant Interactions Aims and scope Submit manuscript

Abstract

Mosquitoes are generally considered nectar thieves that do not contribute to the pollination of the flowers they visit. Here we tested the hypothesis that the common house mosquito, Culex pipiens, contributes to the pollination of tansies, Tanacetum vulgare, and possibly the pollination of other members of the Asteraceae (Achillea millefolium, Leucanthemum vulgare, Solidago canadensis). To test this hypothesis, we (1) field-collected mosquitoes probing inflorescences of T. vulgare, A. millefolium, and L. vulgare, and recorded the number and distribution of pollen grains on their bodies, (2) exposed laboratory-reared Cx. pipiens to inflorescences of T. vulgare, A. millefolium, and S. canadensis, and (3) ran pollination experiments with Cx. pipiens and T. vulgare in a greenhouse. We found (1) that 41 of 164 field-collected Cx. pipiens carried pollen, (2) that 48, 34, and 34 % of Cx. pipiens accumulated pollen from T. vulgare, A. millefolium, and S. canadensis, respectively, during floral visits of greenhouse-grown specimens, and (3) that cross-pollination by Cx. pipiens resulted in significant seed set of T. vulgare in pollination experiments. Based on our observations that Cx. pipiens are frequent floral visitors and are able to carry pollen and to induce seed set in T. vulgare, it is clear that Cx. pipiens plays a role in the pollination of T. vulgare, and possibly other members of the Asteraceae.

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

Similar content being viewed by others

References

  • Andersson IH, Jaenson TGT (1987) Nectar feeding by mosquitoes in Sweden, with special reference to Culex pipiens and Cx. torrentium. Med Vet Entomol 1:59–64

    Article  CAS  PubMed  Google Scholar 

  • Ardö P (1958) On the feeding habits of the Scandinavian mosquitoes. Opusc Entomol 23:171–191

    Google Scholar 

  • Bartareau T, Jackes BR (1994) Some observations on the flowering and pollination of Pterostylus procera M. Clements and D. Jones in North-East Queensland. Orchadian 11:198–201

    Google Scholar 

  • Belton P (1983) The mosquitoes of British Columbia. British Columbia Provincial Museum, Victoria

    Google Scholar 

  • Bosch J, Blas M (1994) Foraging behaviour and pollinating efficiency of Osmia cornuta and Apis mellifera on almond (Hymenoptera, Megachilidae and Apidae). Appl Entomol Zool 29:1–9

    Google Scholar 

  • Brantjes NBM, Leemans JAAM (1976) Silene otites (Caryophyllaceae) pollinated by nocturnal Lepidoptera and mosquitoes. Acta Bot Neerl 25:281–295

    Article  Google Scholar 

  • Britten H (1937) Taeniorrhynchus richardii Fic., and Culex pipiens L. feeding on the flower heads of creeping thistle (Cnicus arvensis Curt.). North West Nat 12:57

    Google Scholar 

  • Bro-Larsen E (1948) Observations on the activity of some culicids. Entomol Medd 25:263–277

    Google Scholar 

  • Cane JH, Schiffhauer D (2003) Dose-response relationships between pollination and fruiting refine pollinator comparisons for cranberry (Vaccinium macrocarpon [Ericaceae]). Am J Bot 90:1425–1432

    Article  PubMed  Google Scholar 

  • Catling PM, Catling VR (1991) A synopsis of breeding systems and pollination in North American orchids. Lindleyana 6:187–210

    Google Scholar 

  • Coleman E (1934) Pollination of Pterostylis acuminate R.BR. and Pterostylis falcata Rogers. Vict Nat 50:248–252

    Google Scholar 

  • Fenster CB, Armbruster WS, Wilson P, Dudash MR, Thomson JD (2004) Pollination syndromes and floral specialization. Ann Rev Ecol Evol Syst 35:375–403

    Article  Google Scholar 

  • Foster WA (1995) Mosquito sugar feeding and reproductive energetics. Ann Rev Entomol 40:443–474

    Article  CAS  Google Scholar 

  • Foster WA, Hancock RG (1994) Nectar-related olfactory and visual attractants for mosquitoes. J Am Mosq Control Assoc 10:288–296

    CAS  PubMed  Google Scholar 

  • Freitas BM (1997) Number and distribution of cashew (Anacardium occidentale) pollen grains on the bodies of its pollinators, Apis mellifera and Centris tarsata. J Apic Res 36:15–22

    Article  Google Scholar 

  • Gorham JR (1976) Orchid pollination by Aedes mosquitoes in Alaska. Am Midl Nat 95:208–210

    Article  Google Scholar 

  • Grimstad PR, DeFoliart GR (1974) Nectar sources of Wisconsin mosquitoes. J Med Entomol 11:331–341

    Article  CAS  PubMed  Google Scholar 

  • Haeger JS (1955) The non-blood feeding habits of Aedes taeniorhynchus (Diptera: Culicidae) on Sanibel Island, Florida. Mosq News 15:21–26

    Google Scholar 

  • Hazlehurst JA, Karubian JO (2016) Nectar robbing impacts pollinator behaviour but not plant reproduction. Oikos. doi:10.1111/oik.03195

    Google Scholar 

  • Healy T, Jepson P (1988) The location of floral nectar sources by mosquitoes: the long-range responses of Anopheles arabiensis Patton (Diptera: Culicidae) to Achillea millefolium flowers and isolated floral odour. Bull Entomol Res 78:651–657

    Article  Google Scholar 

  • Hocking B, Richards WR, Twinn CR (1950) Observations on the bionomics of some northern mosquito species. Can J Res 28D:58–80

    Article  Google Scholar 

  • Hyett J (1960) Pollination of the nodding greenhood. Vic Nat 79:240–241

    Google Scholar 

  • Inouye DW (1980) The terminology of floral larceny. Ecology 61:1251–1253

    Article  Google Scholar 

  • Inouye DW (2010) Mosquitoes: more likely nectar thieves than pollinators. Nature 467:27

    Article  CAS  PubMed  Google Scholar 

  • Irwin RE, Brody AK (1999) Nectar-robbing bumble bees reduce the fitness of Ipomopsis aggregate (Polemoniaceae). Ecology 80:1703–1712

    Article  Google Scholar 

  • Irwin RE, Bronstein JL, Manson JS, Richardson L (2010) Nectar robbing: ecological and evolutionary perspectives. Annu Rev Ecol Evol Syst 41:271–292

    Article  Google Scholar 

  • Irwin RE, Howell P, Galen C (2015) Quantifying direct vs. indirect effects of nectar robbers on male and female components of plant fitness. J Ecol 103:1487–1497

    Article  Google Scholar 

  • Ish-Am G, Eisikowitch D (1993) The behaviour of honey bees (Apis mellifera) visiting avocado (Persea americana) flowers and their contribution to its pollination. J Apic Res 32:175–186

    Article  Google Scholar 

  • Jander R (1976) Grooming and pollen manipulation in bees (Apoidea): the nature and evolution of movements involving the foreleg. Physiol Entomol 1:179–194

    Article  Google Scholar 

  • Jepson P, Healy T (1988) The location of floral nectar sources by mosquitoes: an advanced bioassay for volatile plant odours and initial studies with Aedes aegypti (L.) (Diptera: Culicidae). Bull Entomol Res 78:641–650

    Article  Google Scholar 

  • Jhumur US, Dötterl S, Jürgens A (2007) Electrophysiological and behavioural responses of mosquitoes to volatiles of Silene otites (Caryophyllaceae). Arthropod-Plant Interact 1:245–254

    Article  Google Scholar 

  • Jhumur US, Dötterl S, Jürgens A (2008) Floral odours of Silene otites: their variability and attractiveness to mosquitoes. J Chem Ecol 34:14–25

    Article  CAS  PubMed  Google Scholar 

  • Johnson SD, Midgley JJ (1997) Fly pollination of Gorteria diffusa (Asteraceae), and a possible mimetic function for dark spots on the capitulum. Am J Bot 84:429–436

    Article  CAS  PubMed  Google Scholar 

  • Kevan PG (1972) Insect pollination of high arctic flowers. J Ecol 60:831–847

    Article  Google Scholar 

  • Knab F (1907) Mosquitoes as flower visitors. J N Y Entomol Soc 15:215–219

    Google Scholar 

  • Knudsen JT, Tollsten L (1993) Trends in floral scent chemistry in pollination syndromes: floral scent composition in moth-pollinated taxa. Bot J Linn Soc 113:263–284

    Article  Google Scholar 

  • Kupriyanova ES, Vorotnikova LM (1967) On the ecologo-biological characteristics of a population of Culex pipiens L. in localities near Moscow. Med Parazitol Parazit Bolezni 36:216–224

    Google Scholar 

  • Lara C, Ornelas JF (2001) Nectar “theft” by hummingbird flower mites and its consequences for seed set in Moussonia deppeana. Funct Ecol 15:78–84

    Article  Google Scholar 

  • Lara C, Ornelas JF (2002) Effects of nectar theft by flower mites on hummingbird behaviour and the reproductive success of their host plant, Moussonia deppeana (Gesneriaceae). Oikos 96:470–480

    Article  Google Scholar 

  • Lokki J, Sorsa M, Forsén K, Schantz M (1973) Genetics of monoterpenes in Chrysanthemum vulgare. Hereditas 74:225–232

    Article  CAS  Google Scholar 

  • Luer CA (1975) The native orchids of the United States and Canada, excluding Florida. W.S. Cromwell, Ipswich

    Google Scholar 

  • Magnarelli LA (1977) Nectar feeding by Aedes sollicitans and its relation to gonotrophic activity. Environ Entomol 6:237–242

    Article  Google Scholar 

  • Magnarelli LA (1978) Bionomics of the salt-marsh mosquito, Aedes cantator (Diptera: Culicidae). Environ Entomol 7:512–517

    Article  Google Scholar 

  • Magnarelli LA (1983) Nectar sugars and caloric reserves in natural populations of Aedes canadensis and Aedes stimulans (Diptera: Culicidae). Environ Entomol 12:1482–1486

    Article  Google Scholar 

  • Mauer DJ, Rowley WA (1999) Attraction of Culex pipiens pipiens (Diptera: Culicidae) to flower volatiles. J Med Entomol 36:503–507

    Article  CAS  PubMed  Google Scholar 

  • Moore PD, Webb JA, Collinson ME (1991) Pollen analysis, 2nd edn. Blackwell, Oxford

    Google Scholar 

  • Müller H (1873) Die Befruchtung der Blumen durch Insekten. Wilhelm Engelmann, Leipzig, pp 197–198

    Book  Google Scholar 

  • Neff JL, Simpson BB (1990) The roles of phenology and reward structure in the pollination biology of wild sunflower (Helionathus annus L., Asteraceae). Isr J Bot 39:197–216

    Google Scholar 

  • Norment CJ (1988) The effect of nectar-thieving ants on the reproductive success of Frasera speciose (Gentianaceae). Am Midl Nat 120:331–336

    Article  Google Scholar 

  • Nyasembe VO, Teal PEA, Mukabana WR, Tumlinson JH, Torto B (2012) Behavioural response of the malaria vector Anopheles gambiae to host plant volatiles and synthetic blends. Parasit Vectors 5:234

    Article  PubMed  PubMed Central  Google Scholar 

  • Olsen KM (1997) Pollination effectiveness and pollinator importance in a population of Heterotheca subaxillaris (Asteraceae). Oecologia 109:114–121

    Google Scholar 

  • Orford KA, Vaughan IP, Memmott J (2015) The forgotten flies: the importance of non-syrphid Diptera as pollinators. Proc R Soc B Biol Sci 282:20142934

    Article  Google Scholar 

  • Ortega-Olivencia A, Rodríguez-Riaño T, Valtueña FJ, López J, Devesa JA (2005) First confirmation of a native bird-pollinated plant in Europe. Oikos 110:578–590

    Article  Google Scholar 

  • Otienoburu PE, Ebrahimi B, Phelan PL, Foster WA (2012) Analysis and optimization of a synthetic milkweed floral attractant for mosquitoes. J Chem Ecol 38:873–881

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Patt JM, Merchant MW, Williams DRE, Meeuse BJD (1989) Pollination biology of Platanthera stricta (Orchidaceae) in Olympic National Park, Washington. Am J Bot 76:1097–1106

    Article  Google Scholar 

  • Philip C (1943) Flowers as a suggested source of mosquitoes during encephalitis studies, and incidental mosquito records in the Dakotas in 1941. J Parasitol 29:328–329

    Article  Google Scholar 

  • Sandholm HA, Price RD (1962) Field observations on the nectar feeding habits of some Minnesota mosquitoes. Mosq News 22:346–349

    Google Scholar 

  • Smith SM, Gadawski RM (1994) Nectar feeding by the early-spring mosquito Aedes provocans. Med Vet Entomol 8:201–213

    Article  CAS  PubMed  Google Scholar 

  • Stoutamire WP (1968) Mosquito pollination of Habenaria obtusata (Orchidaceae). Mich Bot 7:203–212

    Google Scholar 

  • Stoutamire WP (1971) Pollination in temperate American orchids. In: Corrigan MJ (ed) Proceedings of the sixth World orchid conference. Halstead Press, Sydney, Australia, pp 233–243

  • Thielman AC, Hunter FF (2007) A photographic key to adult female mosquito species of Canada (Diptera: Culicidae). Can J Arthropod Identif 4:1–116

    Google Scholar 

  • Thien LB (1969) Mosquito pollination of Habenaria obtusata (Orchidaceae). Am J Bot 56:232–237

    Article  Google Scholar 

  • Uemura S, Ohkawara K, Kudo G, Wada N, Higashi S (1993) Heat-production and cross-pollination of the Asian skunk cabbage Symplocarpus renifolius (Araceae). Am J Bot 80:635–640

    Article  Google Scholar 

  • Vargo AM, Foster WA (1982) Responsiveness of female Aedes aegypti to flower extracts. J Med Entomol 19:710–718

    Article  Google Scholar 

  • Vinogradova EB (2000) Culex pipiens pipiens mosquitoes: taxonomy, distribution, ecology, physiology, genetics, applied importance and control. Pensoft, Moscow

    Google Scholar 

  • Waser NM, Chittka L, Price MV, Williams NM, Ollerton J (1996) Generalization in pollination systems, and why it matters. Ecology 77:1043–1060

    Article  Google Scholar 

  • Whitehead MR, Peakall R (2009) Integrating floral scent, pollination ecology, and population genetics. Funct Ecol 23:863–874

    Article  Google Scholar 

  • Wood DM, Dang PT, Ellis RA (1979) The insects and arachnids of Canada, part 6, the mosquitoes of Canada. Canadian Government Publishing Centre, Ottawa

    Google Scholar 

  • Yee WL, Foster WA, Howe MJ, Hancock RG (1992) Simultaneous field comparison of evening temporal distributions of nectar and blood feeding by Aedes vexans and Ae. trivittatus (Diptera: Culicidae) in Ohio. J Med Entomol 29:356–360

    Article  CAS  PubMed  Google Scholar 

  • Zhang YW, Zhao JM, Iouye DW (2014) Nectar thieves influence reproductive fitness by altering behaviour of nectar robbers and legitimate pollinators in Corydalis ambigua (Fumariaceae). J Ecol 102:229–237

    Article  Google Scholar 

Download references

Acknowledgments

We thank Michael Hrabar for mosquito photographs, Rolf Mathewes for assistance with pollen identification and botanical terminology, Elizabeth Elle for feedback, Heather Coatsworth and Joyce Leung for assistance collecting mosquito specimens, Sharon Oliver for discussion, and two anonymous reviewers for constructive comments. The research was supported by scholarships to DP (Master of Pest Management Graduate Entrance Scholarship, CD Nelson Memorial Entrance Scholarship, Sharon Clements Biological Science Award, Simon Fraser University Graduate Fellowships, Thelma Finlayson Graduate Fellowship, Provost’s Prize of Distinction), and by a Natural Sciences and Engineering Research Council of Canada—Industrial Research Chair to GG—with Scotts Canada Ltd. as the industrial sponsor.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Daniel A. H. Peach.

Additional information

Handling Editor: Kristine Nemec.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Peach, D.A.H., Gries, G. Nectar thieves or invited pollinators? A case study of tansy flowers and common house mosquitoes. Arthropod-Plant Interactions 10, 497–506 (2016). https://doi.org/10.1007/s11829-016-9445-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11829-016-9445-9

Keywords

Navigation