Restricted access
Research articles
Research articlesNocturnal pollinators strongly contribute to pollen transport of wild flowers in an agricultural landscape
Published:13 May 2020https://doi.org/10.1098/rsbl.2019.0877
Abstract
Dramatic declines in diurnal pollinators have created great scientific interest in plant–pollinator relationships and associated pollination services. Existing literature, however, is generally focused on diurnal pollinating insect taxa, especially on Apidae (Hymenoptera) and Syrphidae (Diptera) pollinators, while nocturnal macro-moths that comprise extremely species-rich flower-visiting families have been largely neglected. Here, we report that in agricultural landscapes, macro-moths can provide unique, highly complex pollen transport links, making them vital components of overall wild plant–pollinator networks in agro-ecosystems. Pollen transport occurred more frequently on the moths' ventral thorax rather than on their mouthparts that have been traditionally targeted for pollen swabbing. Pollen transport loads suggest that nocturnal moths contribute key pollination services for several wild plant families in agricultural landscapes, in addition to providing functional resilience to diurnal networks. Severe declines in richness and abundance of settling moth populations highlight the urgent need to include them in future management and conservation strategies within agricultural landscapes.
Footnotes
References
- 1.
Klein A-M, Vaissiere BE, Cane JH, Steffan-Dewenter I, Cunningham SA, Kremen C, Tscharntke T . 2007Importance of pollinators in changing landscapes for world crops. Proc. R. Soc. B 274, 303-313. (doi:10.1098/rspb.2006.3721) Link, ISI, Google Scholar - 2.
Goulson D, Lye GC, Darvill B . 2008Decline and conservation of bumble bees. Annu. Rev. Entomol. 53, 191-208. (doi:10.1146/annurev.ento.53.103106.093454) Crossref, PubMed, ISI, Google Scholar - 3.
Potts SG 2016The assessment report on pollinators, pollination and food production: summary for policymakers. Bonn, Germany: Secretariat of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services. Google Scholar - 4.
Michener CD . 2000The bees of the world. Baltimore, MD: Johns Hopkins University Press. Google Scholar - 5.
Thompson FC . 2013Family Syrphidae. In Systema dipterorum, version 15 (edsPape T, Thompson FC ). See http://www.diptera.org (accessed 3 January 2019). Google Scholar - 6.
van Nieukerken EJ 2011Order Lepidoptera Linnaeus, 1758. Zootaxa 3148, 212-221. (doi:10.11646/zootaxa.3148.1.39) Crossref, Google Scholar - 7.
Cordeiro GD, Pinheiro M, Dötterl S, Alves-dos-Santos I . 2017Pollination of Campomanesia phaea (Myrtaceae) by night-active bees: a new nocturnal pollination system mediated by floral scent. Plant Biol. 19, 132-139. (doi:10.1111/plb.12520) Crossref, PubMed, ISI, Google Scholar - 8.
Krug C, Cordeiro GD, Schäffler I, Silva CI, Oliveira R, Schlindwein C, Dötterl S, Alves-dos-Santos I . 2018Nocturnal bee pollinators are attracted to guarana flowers by their scents. Front. Plant Sci. 9, 1-6. (doi:10.3389/fpls.2018.01072) Crossref, PubMed, ISI, Google Scholar - 9.
Devoto M, Bailey S, Memmott J . 2011The ‘night shift’: nocturnal pollen-transport networks in a boreal pine forest. Ecol. Entomol. 36, 25-35. (doi:10.1111/j.1365-2311.2010.01247.x) Crossref, ISI, Google Scholar - 10.
Banza P, Belo ADF, Evans DM . 2015The structure and robustness of nocturnal lepidopteran pollen-transfer networks in a biodiversity hotspot. Insect Conserv. Divers. 8, 538-546. (doi:10.1111/icad.12134) Crossref, ISI, Google Scholar - 11.
Macgregor CJ, Evans DM, Fox R, Pocock MJO . 2017The dark side of street lighting: impacts on moths and evidence for the disruption of nocturnal pollen transport. Glob. Change Biol. 23, 697-707. (doi:10.1111/gcb.13371) Crossref, PubMed, ISI, Google Scholar - 12.
Knop E, Zoller L, Ryser R, Erpe CG, Horler M, Fontaine C . 2017Artificial light at night as a new threat to pollination. Nature 548, 206-209. (doi:10.1038/nature23288) Crossref, PubMed, ISI, Google Scholar - 13.
Macgregor CJ, Kitson JJN, Fox R, Hahn C, Lunt DH, Pocock MJO, Evans DM . 2019Construction, validation and application of nocturnal pollen transport networks in an agro-ecosystem: a comparison using microscopy and DNA metabarcoding. Ecol. Entomol. 44, 17-29. (doi:10.1111/een.12674) Crossref, ISI, Google Scholar - 14.
Banza P, Macgregor CJ, Belo ADF, Fox R, Pocock MJO, Evans DM . 2019Wildfire alters the structure and seasonal dynamics of nocturnal pollen-transport networks. Funct. Ecol. 33, 1882-1892. (doi:10.1111/1365-2435.13388) Crossref, ISI, Google Scholar - 15.
Adler LS, Irwin RE . 2006Comparison of pollen transfer dynamics by multiple floral visitors: experiments with pollen and fluorescent dye. Ann. Bot. 97, 141-150. (doi:10.1093/aob/mcj012) Crossref, PubMed, ISI, Google Scholar - 16.
Rader R, Howlett BG, Cunningham SA, Westcott DA, Newstrom-Lloyd LE, Walker MK, Teulon DAJ, Edwards W . 2009Alternative pollinator taxa are equally efficient but not as effective as the honeybee in a mass flowering crop. J. Appl. Ecol. 46, 1080-1087. (doi:10.1111/j.1365-2664.2009.01700.x) Crossref, ISI, Google Scholar - 17.
Seeley T, Camazine S, Sneyd J . 1991Collective decision-making in honey bees: how colonies choose among nectar sources. Behav. Ecol. Sociobiol. 28, 277-290. (doi:10.1007/BF00175101) Crossref, ISI, Google Scholar - 18.
Cnaani J, Thomson JD, Papaj DR . 2006Flower choice and learning in foraging bumblebees: effects of variation in nectar volume and concentration. Ethology 112, 278-285. (doi:10.1111/j.1439-0310.2006.01174.x) Crossref, ISI, Google Scholar - 19.
Ruedenauer FA, Spaethe J, Leonhardt SD . 2016Hungry for quality-individual bumblebees forage flexibly to collect high-quality pollen. Behav. Ecol. Sociobiol. 70, 1209-1217. (doi:10.1007/s00265-016-2129-8) Crossref, ISI, Google Scholar - 20.
Rose F, O'Reilly C . 2006The wild flower key: how to identify wild flowers, trees, and shrubs in britain and Ireland, 2nd edn. London, UK: Penguin Group. Google Scholar - 21.
Beattie A . 1972A technique for the study of insect-borne pollen. Pan-Pacific Entomol. 47, 82. ISI, Google Scholar - 22.
Moore PD, Webb JA, Collinson ME . 1991Pollen analysis, 2nd edn. Oxford, UK: Blackwell Science Ltd. Google Scholar - 23.
Stubbs A, Falk S . 2002British hoverflies: an illustrated identification guide, 2nd edn. Reading, UK: British Entomological & Natural History Society. Google Scholar - 24.
Waring P, Townsend M. 2004Field guide to the moths of Great Britain and Ireland. Rotherwick, UK: British Wildlife Publishing. Google Scholar - 25.
Thomas J, Lewington R . 2014The butterflies of Britain and Ireland, 3rd edn. Totnes, UK: British Wildlife Publishing. Google Scholar - 26.
Falk S . 2015Field Guide to bees of Great Britain and Ireland. Totnes, UK: British Wildlife Publishing. Google Scholar - 27.
Kearns CA, Inouye DW . 1993Techniques for pollination biologists. Niwot, CO: University Press of Colorado. Google Scholar - 28.
Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D . 2018vegan: Community Ecology Package. See https://cran.R-project.org/package=vegan Google Scholar - 29.
Dormann CF, Gruber B, Fründ J . 2008Introducing the bipartite package: analysing ecological networks. R news 8/2, 8-11. Google Scholar - 30.
Bosch J, Martín González AM, Rodrigo A, Navarro D . 2009Plant–pollinator networks: adding the pollinator's perspective. Ecol. Lett. 12, 409-419. (doi:10.1111/j.1461-0248.2009.01296.x) Crossref, PubMed, ISI, Google Scholar - 31.
King C, Ballantyne G, Willmer PG . 2013Why flower visitation is a poor proxy for pollination: measuring single-visit pollen deposition, with implications for pollination networks and conservation. Methods Ecol. Evol. 4, 811-818. (doi:10.1111/2041-210X.12074) Crossref, ISI, Google Scholar - 32.
Batra SWT . 1979Insects associated with weeds in the northeastern United States. III. Chickweed, Stellaria media, and stitchwort, S. graminea (Caryophyllaceae). J. New York Entomol. S. 87, 223-235. Google Scholar - 33.
Cruden RW, McClain AM, Shrivastava GP . 1996Pollination biology and breeding system of Alliaria petiolata (Brassicaceae). B. Torr. Bot. Club 123, 273-280. (doi:10.2307/2996775) Crossref, Google Scholar - 34.
Donnelly SE, Lortie CJ, Aarssen LW . 1998Pollination in Verbascum thapsus (Scrophulariaceae): the advantage of being tall. Am. J. Bot. 85, 1618-1625. (doi:10.2307/2446490) Crossref, PubMed, ISI, Google Scholar - 35.
Memmott J . 1999The structure of a plant–pollinator food web. Ecol. Lett. 2, 276-280. (doi:10.1046/j.1461-0248.1999.00087.x) Crossref, ISI, Google Scholar - 36.
Taylor K, Rowland P . 2011Biological flora of the British Isles: Stachys palustris L. J Ecol. 99, 1081-1090. (doi:10.1111/j.1365-2745.2011.01849.x) Crossref, ISI, Google Scholar - 37.
Stanley DA, Stout JC . 2014Pollinator sharing between mass-flowering oilseed rape and co-flowering wild plants: implications for wild plant pollination. Plant Ecol. 215, 315-325. (doi:10.1007/s11258-014-0301-7) Crossref, ISI, Google Scholar - 38.
Orford KA, Murray PJ, Vaughan IP, Memmott J . 2016Modest enhancements to conventional grassland diversity improve the provision of pollination services. J. Appl. Ecol. 53, 906-915. (doi:10.1111/1365-2664.12608) Crossref, PubMed, ISI, Google Scholar - 39.
Stewart RIA, Andersson GKS, Brönmark C, Klatt BK, Hansson L-A, Zülsdorff V, Smith HG . 2017Ecosystem services across the aquatic–terrestrial boundary: linking ponds to pollination. Basic Appl. Ecol. 18, 13-20. (doi:10.1016/j.baae.2016.09.006) Crossref, ISI, Google Scholar - 40.
Willmer P. 2011Pollination by butterflies and moths. In Pollination and floral ecology, pp. 322-336. Princeton, NJ: Princeton University Press. Crossref, Google Scholar - 41.
Atwater MM . 2013Diversity and nectar hosts of flower-settling moths within a Florida sandhill ecosystem. J. Nat. Hist. 47, 2719-2734. (doi:10.1080/00222933.2013.791944) Crossref, ISI, Google Scholar - 42.
LeCroy KA, Shew HW, van Zandt PA. 2013Pollen presence on nocturnal moths in the Ketona Dolomite glades of Bibb County, Alabama. Southern Lepidopterists' News 35, 136-142. Google Scholar - 43.
Funamoto D . 2019Precise sternotribic pollination by settling moths in Adenophora maximowicziana (Campanulaceae). Int. J. Plant Sci. 180, 200-208. (doi:10.1086/701734) Crossref, ISI, Google Scholar - 44.
Morais M, Moreira L, Feas X, Estevinho LM . 2011Honeybee-collected pollen from five Portuguese natural parks: palynological origin, phenolic content, antioxidant properties and antimicrobial activity. Food Chem. Toxicol. 49, 1096-1101. (doi:10.1016/j.fct.2011.01.020) Crossref, PubMed, ISI, Google Scholar - 45.
Conrad KF, Warren MS, Fox R, Parsons MS, Woiwod IP . 2006Rapid declines of common, widespread British moths provide evidence of an insect biodiversity crisis. Biol. Conserv. 132, 279-291. (doi:10.1016/j.biocon.2006.04.020) Crossref, ISI, Google Scholar - 46.
Sutrisno H . 2010The impact of human activities to dynamic of insect communities: a case study in Gunung Salak, West Java. HAYATI J. Biosci. 17, 161-166. (doi:10.4308/hjb.17.4.161) Crossref, Google Scholar - 47.
Groenendijk D, Ellis WN . 2011The state of the Dutch larger moth fauna. J. Insect Conserv. 15, 95-101. (doi:10.1007/s10841-010-9326-y) Crossref, ISI, Google Scholar - 48.
Young BE, Auer S, Ormes M, Rapacciuolo G, Schweitzer D, Sears N . 2017Are pollinating hawk moths declining in the Northeastern United States? An analysis of collection records. PLoS ONE 12, e0185683. (doi:10.1371/journal.pone.0185683) Crossref, PubMed, ISI, Google Scholar - 49.
Macgregor CJ, Williams JH, Bell JR, Thomas CD . 2019Moth biomass increases and decreases over 50 years in Britain. Nat. Ecol. Evol. 3, 1645-1649. (doi:10.1038/s41559-019-1028-6) Crossref, PubMed, ISI, Google Scholar - 50.
Kadlec T, Kotela MAAM, Novak I, Konvicka M, Jarosik V . 2009Effect of land use and climate on the diversity of moth guilds with different habitat specialization. Community Ecol. 10, 152-158. (doi:10.1556/ComEc.10.2009.2.3) Crossref, ISI, Google Scholar - 51.
Botham MS, Fernandez-Ploquin EC, Brereton T, Harrower CA, Roy DB, Heard MS . 2015Lepidoptera communities across an agricultural gradient: how important are habitat area and habitat diversity in supporting high diversity?J. Insect Conserv. 19, 403-420. (doi:10.1007/s10841-015-9760-y) Crossref, ISI, Google Scholar - 52.
Merckx T, Marini L, Feber RE, Macdonald DW . 2012Hedgerow trees and extended-width field margins enhance macro-moth diversity: implications for management. J. Appl. Ecol. 49, 1396-1404. (doi:10.1111/j.1365-2664.2012.02211.x) Crossref, ISI, Google Scholar - 53.
Alison J, Duffield SJ, Morecroft MD, Marrs RH, Hodgson JA . 2017Successful restoration of moth abundance and species-richness in grassland created under agri-environment schemes. Biol. Conserv. 213, 51-58. (doi:10.1016/j.biocon.2017.07.003) Crossref, ISI, Google Scholar
