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.
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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
Ardö P (1958) On the feeding habits of the Scandinavian mosquitoes. Opusc Entomol 23:171–191
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
Belton P (1983) The mosquitoes of British Columbia. British Columbia Provincial Museum, Victoria
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
Brantjes NBM, Leemans JAAM (1976) Silene otites (Caryophyllaceae) pollinated by nocturnal Lepidoptera and mosquitoes. Acta Bot Neerl 25:281–295
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
Bro-Larsen E (1948) Observations on the activity of some culicids. Entomol Medd 25:263–277
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
Catling PM, Catling VR (1991) A synopsis of breeding systems and pollination in North American orchids. Lindleyana 6:187–210
Coleman E (1934) Pollination of Pterostylis acuminate R.BR. and Pterostylis falcata Rogers. Vict Nat 50:248–252
Fenster CB, Armbruster WS, Wilson P, Dudash MR, Thomson JD (2004) Pollination syndromes and floral specialization. Ann Rev Ecol Evol Syst 35:375–403
Foster WA (1995) Mosquito sugar feeding and reproductive energetics. Ann Rev Entomol 40:443–474
Foster WA, Hancock RG (1994) Nectar-related olfactory and visual attractants for mosquitoes. J Am Mosq Control Assoc 10:288–296
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
Gorham JR (1976) Orchid pollination by Aedes mosquitoes in Alaska. Am Midl Nat 95:208–210
Grimstad PR, DeFoliart GR (1974) Nectar sources of Wisconsin mosquitoes. J Med Entomol 11:331–341
Haeger JS (1955) The non-blood feeding habits of Aedes taeniorhynchus (Diptera: Culicidae) on Sanibel Island, Florida. Mosq News 15:21–26
Hazlehurst JA, Karubian JO (2016) Nectar robbing impacts pollinator behaviour but not plant reproduction. Oikos. doi:10.1111/oik.03195
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
Hocking B, Richards WR, Twinn CR (1950) Observations on the bionomics of some northern mosquito species. Can J Res 28D:58–80
Hyett J (1960) Pollination of the nodding greenhood. Vic Nat 79:240–241
Inouye DW (1980) The terminology of floral larceny. Ecology 61:1251–1253
Inouye DW (2010) Mosquitoes: more likely nectar thieves than pollinators. Nature 467:27
Irwin RE, Brody AK (1999) Nectar-robbing bumble bees reduce the fitness of Ipomopsis aggregate (Polemoniaceae). Ecology 80:1703–1712
Irwin RE, Bronstein JL, Manson JS, Richardson L (2010) Nectar robbing: ecological and evolutionary perspectives. Annu Rev Ecol Evol Syst 41:271–292
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
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
Jander R (1976) Grooming and pollen manipulation in bees (Apoidea): the nature and evolution of movements involving the foreleg. Physiol Entomol 1:179–194
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
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
Jhumur US, Dötterl S, Jürgens A (2008) Floral odours of Silene otites: their variability and attractiveness to mosquitoes. J Chem Ecol 34:14–25
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
Kevan PG (1972) Insect pollination of high arctic flowers. J Ecol 60:831–847
Knab F (1907) Mosquitoes as flower visitors. J N Y Entomol Soc 15:215–219
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
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
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
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
Lokki J, Sorsa M, Forsén K, Schantz M (1973) Genetics of monoterpenes in Chrysanthemum vulgare. Hereditas 74:225–232
Luer CA (1975) The native orchids of the United States and Canada, excluding Florida. W.S. Cromwell, Ipswich
Magnarelli LA (1977) Nectar feeding by Aedes sollicitans and its relation to gonotrophic activity. Environ Entomol 6:237–242
Magnarelli LA (1978) Bionomics of the salt-marsh mosquito, Aedes cantator (Diptera: Culicidae). Environ Entomol 7:512–517
Magnarelli LA (1983) Nectar sugars and caloric reserves in natural populations of Aedes canadensis and Aedes stimulans (Diptera: Culicidae). Environ Entomol 12:1482–1486
Mauer DJ, Rowley WA (1999) Attraction of Culex pipiens pipiens (Diptera: Culicidae) to flower volatiles. J Med Entomol 36:503–507
Moore PD, Webb JA, Collinson ME (1991) Pollen analysis, 2nd edn. Blackwell, Oxford
Müller H (1873) Die Befruchtung der Blumen durch Insekten. Wilhelm Engelmann, Leipzig, pp 197–198
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
Norment CJ (1988) The effect of nectar-thieving ants on the reproductive success of Frasera speciose (Gentianaceae). Am Midl Nat 120:331–336
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
Olsen KM (1997) Pollination effectiveness and pollinator importance in a population of Heterotheca subaxillaris (Asteraceae). Oecologia 109:114–121
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
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
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
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
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
Sandholm HA, Price RD (1962) Field observations on the nectar feeding habits of some Minnesota mosquitoes. Mosq News 22:346–349
Smith SM, Gadawski RM (1994) Nectar feeding by the early-spring mosquito Aedes provocans. Med Vet Entomol 8:201–213
Stoutamire WP (1968) Mosquito pollination of Habenaria obtusata (Orchidaceae). Mich Bot 7:203–212
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
Thien LB (1969) Mosquito pollination of Habenaria obtusata (Orchidaceae). Am J Bot 56:232–237
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
Vargo AM, Foster WA (1982) Responsiveness of female Aedes aegypti to flower extracts. J Med Entomol 19:710–718
Vinogradova EB (2000) Culex pipiens pipiens mosquitoes: taxonomy, distribution, ecology, physiology, genetics, applied importance and control. Pensoft, Moscow
Waser NM, Chittka L, Price MV, Williams NM, Ollerton J (1996) Generalization in pollination systems, and why it matters. Ecology 77:1043–1060
Whitehead MR, Peakall R (2009) Integrating floral scent, pollination ecology, and population genetics. Funct Ecol 23:863–874
Wood DM, Dang PT, Ellis RA (1979) The insects and arachnids of Canada, part 6, the mosquitoes of Canada. Canadian Government Publishing Centre, Ottawa
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
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
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.
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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
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DOI: https://doi.org/10.1007/s11829-016-9445-9