Using functional traits to predict pollination services: A review

Authors

DOI:

https://doi.org/10.26786/1920-7603(2023)735

Keywords:

Pollination, Effect traits, Ecosystem service, Functional diversity, Review

Abstract

Pollination is a fundamental ecosystem service. Predictive and mechanistic models linking pollinator community structure to pollination services increasingly incorporate information on unique functional differences among species, so called effects traits.   There is little consensus as to which traits are most important in supporting pollination services at either an individual or community level. Here, we synthesise the state of current knowledge regarding the role and efficacy of traits for predicting pollination, as well as the use of different methods for describing the trait structure of pollinator assemblages. We find a wide range of traits are currently used to predict pollination services, including morphological, behavioural and phenological characteristics. However, we show that the evidence demonstrating their importance is often limited or mixed. There is a trade-off in how traits are used between those that are easier to measure, available for many species but have only limited evidence for their role in pollination, vs. those that are harder to measure but with a more robust link with pollination service delivery.   We highlight how community weighted means and measures of functional diversity offer important, albeit different insights into pollination service delivery. We discuss how their relative importance is likely to depend on the goals of the study. To maximise fully the utilisation of traits to predict pollination services, future research should be directed towards the widespread and consistent validation of the links among different traits and the pollination service across crop and semi-natural plant communities. Ideally this also needs to address geographical and taxonomic biases in trait collection.

Author Biographies

Arran Greenop

 

 

Richard F. Pywell

 

 

References

Bartomeus I., Ascher JS, Gibbs, J, Danforth, BN, Wagner, DL, Hedtke, SM Winfree R (2013) Historical changes in northeastern US bee pollinators related to shared ecological traits. Proceedings of the National Academy of Sciences 110: 4656-4660. https://doi.org/10.1073/pnas.1218503110 DOI: https://doi.org/10.1073/pnas.1218503110

Bartomeus I, Cariveau DP, Harrison T, Winfree R (2018) On the inconsistency of pollinator species traits for predicting either response to land-use change or functional contribution. Oikos 127: 306-315. https://doi.org/10.1111/oik.04507 DOI: https://doi.org/10.1111/oik.04507

Blitzer EJ, Gibbs J, Park MG, Danforth BN (2016) Pollination services for apple are dependent on diverse wild bee communities. Agriculture, Ecosystems and Environment 221: 1-7. https://doi.org/10.1016/j.agee.2016.01.004 DOI: https://doi.org/10.1016/j.agee.2016.01.004

Bommarco R, Biesmeijer JC, Meyer B, Potts SG, Pöyry J, Roberts, SPM, Steffan-Dewenter I, Öckinger E (2010) Dispersal capacity and diet breadth modify the response of wild bees to habitat loss. Proceedings of the Royal Society B: Biological Sciences 277: 2075-2082. https://doi.org/10.1098/rspb.2009.2221 DOI: https://doi.org/10.1098/rspb.2009.2221

Borges RC, Padovani K, Imperatriz-Fonseca VL, Giannini TC (2020) A dataset of multi-functional ecological traits of Brazilian bees. Scientific Data 7: 1-9. https://doi.org/10.1038/s41597-020-0461-3 DOI: https://doi.org/10.1038/s41597-020-0461-3

Brittain C, Kremen C, Klein A-M (2013a) Biodiversity buffers pollination from changes in environmental conditions. Global Change Biology 19: 540-547. https://doi.org/10.1111/gcb.12043 DOI: https://doi.org/10.1111/gcb.12043

Brittain C, Williams N, Kremen C, Klein A-M (2013b) Synergistic effects of non-Apis bees and honey bees for pollination services. Proceedings of the Royal Society B: Biological Sciences 280: 20122767. https://doi.org/10.1098/rspb.2012.2767 DOI: https://doi.org/10.1098/rspb.2012.2767

Brosi BJ, Briggs HM (2013) Single pollinator species losses reduce floral fidelity and plant reproductive function. Proceedings of the National Academy of Sciences 110: 13044-13048. https://doi.org/10.1073/pnas.1307438110 DOI: https://doi.org/10.1073/pnas.1307438110

Carmona CP, Bello F de, Mason NWH, Lepš J (2019) Trait probability density (TPD): measuring functional diversity across scales based on TPD with R. Ecology 100: e02876. https://doi.org/10.1002/ecy.2876 DOI: https://doi.org/10.1002/ecy.2876

Chole H, Woodard SH, Bloch G (2019) Body size variation in bees: regulation, mechanisms, and relationship to social organization. Current Opinion in Insect Science 35: 77-87. https://doi.org/10.1016/j.cois.2019.07.006 DOI: https://doi.org/10.1016/j.cois.2019.07.006

Elzay SD, Baum KA (2021) Landscape characteristics predict body sizes in wild bees: implications for pollination services and foraging range. Journal of Insect Conservation 25: 243-253. https://doi.org/10.1007/s10841-021-00294-y DOI: https://doi.org/10.1007/s10841-021-00294-y

Falk S, Lewington R (2016) Field Guide to the Bees of Great Britain and Ireland. Bloomsbury Wildlife, London.

Fijen TPM, Scheper JA, Boom TM, Janssen N, Raemakers I, Kleijn D (2018) Insect pollination is at least as important for marketable crop yield as plant quality in a seed crop. Ecology Letters 21: 1704-1713. https://doi.org/10.1111/ele.13150 DOI: https://doi.org/10.1111/ele.13150

Földesi R, Howlett BG, Grass I, Batáry P (2020) Larger pollinators deposit more pollen on stigmas across multiple plant species - A meta‐analysis. Journal of Applied Ecology 10.1111/1365-2664.13798. https://doi.org/10.1111/1365-2664.13798 DOI: https://doi.org/10.1111/1365-2664.13798

Fründ J, Dormann CF, Holzschuh A, Tscharntke T (2013) Bee diversity effects on pollination depend on functional complementarity and niche shifts. Ecology 94: 2042-2054. https://doi.org/10.1890/12-1620.1 DOI: https://doi.org/10.1890/12-1620.1

Gagic V, Bartomeus I, Jonsson T, Taylor A, Winqvist C, Fischer C, Slade EM, Steffan-Dewenter I, Emmerson M, Potts SG, Tscharntke T, Weisser W, Bommarco R (2015) Functional identity and diversity of animals predict ecosystem functioning better than species-based indices. Proceedings of the Royal Society B: Biological Sciences 282: 20142620. https://doi.org/10.1098/rspb.2014.2620 DOI: https://doi.org/10.1098/rspb.2014.2620

Garibaldi LA, Bartomeus I, Bommarco R, Klein AM, Cunningham, SA, Aizen MA, Boreux V, Garratt MD, Carvalheiro LG, Kremen C, Morales CL, Schuepp C, Chacoff NP, Freitas BM, Gagic V, Holzschuh A, Klatt BK, Krewenka KM, Krishnan S, Mayfield MM, Motzke I, Otieno M, Petersen J, Potts SG, Ricketts TH, Rundlof M, Sciligo A, Sinu PA, Steffan-Dewenter I, Taki H, Tscharntke T, Vergara CH, Viana B F, Woyciechowski, M. (2015) Trait matching of flower visitors and crops predicts fruit set better than trait diversity. Journal of Applied Ecology, 52: 1436-1444. https://doi.org/10.1111/1365-2664.12530 DOI: https://doi.org/10.1111/1365-2664.12530

Garratt MPD, Bishop J, Degani E, Potts SG, Shaw RF, Shi A, et al. (2018) Insect pollination as an agronomic input: Strategies for oilseed rape production. Journal of Applied Ecology 55: 2834-2842. https://doi.org/10.1111/1365-2664.13153 DOI: https://doi.org/10.1111/1365-2664.13153

Gómez JM, Abdelaziz M, Lorite J, Jesús Muñoz-Pajares A., Perfectti F (2010) Changes in pollinator fauna cause spatial variation in pollen limitation. Journal of Ecology 98: 1243-1252. https://doi.org/10.1111/j.1365-2745.2010.01691.x DOI: https://doi.org/10.1111/j.1365-2745.2010.01691.x

Goulson D (1999) Foraging strategies of insects for gathering nectar and pollen, and implications for plant ecology and evolution. Perspectives in Plant Ecology Evolution and Systematics 2: 185-209. https://doi.org/10.1078/1433-8319-00070 DOI: https://doi.org/10.1078/1433-8319-00070

Goulson D, Nicholls E, Botías C, Rotheray EL (2015) Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science 347: 1255957. https://doi.org/10.1126/science.1255957 DOI: https://doi.org/10.1126/science.1255957

Higashi S, Ohara M, Arai H, Matsuo K (1988). Robber-like pollinators: overwintered queen bumblebees foraging on Corydalis ambigua. Ecological Entomology 13:411-418. https://doi.org/10.1111/j.1365-2311.1988.tb00373.x DOI: https://doi.org/10.1111/j.1365-2311.1988.tb00373.x

Greenop A, Woodcock BA, Outhwaite CL, Carvell C, Pywell RF, Mancini F, Edwards FK, Johnson AC, Isaac NJB (2021) Patterns of invertebrate functional diversity highlight the vulnerability of ecosystem services over a 45-year period. Current Biology 31: 4627-4634. https://doi.org/10.1016/j.cub.2021.07.080 DOI: https://doi.org/10.1016/j.cub.2021.07.080

Greenwell MP, Brereton T, Day JC, Roy B., Oliver TH (2019) Predicting resilience of ecosystem functioning from co‐varying species' responses to environmental change. Ecology and Evolution 9: 11775-11790. https://doi.org/10.1002/ece3.5679 DOI: https://doi.org/10.1002/ece3.5679

Grime JP (1998) Benefits of plant diversity to ecosystems: immediate, filter and founder effects. Journal of Ecology 86: 902-910. https://doi.org/10.1046/j.1365-2745.1998.00306.x DOI: https://doi.org/10.1046/j.1365-2745.1998.00306.x

Hoehn P, Tscharntke T, Tylianakis JM, Steffan-Dewenter I (2008) Functional group diversity of bee pollinators increases crop yield. Proceedings of the Royal Society B: Biological Sciences 275: 2283-2291. https://doi.org/10.1098/rspb.2008.0405 DOI: https://doi.org/10.1098/rspb.2008.0405

Jauker F, Speckmann M, Wolters V (2016) Intra-specific body size determines pollination effectiveness. Basic and Applied Ecology 17: 714-719. https://doi.org/10.1016/j.baae.2016.07.004 DOI: https://doi.org/10.1016/j.baae.2016.07.004

Kendall DA, Smith BD (1975) The Pollinating Efficiency of Honeybee and Bumblebee Visits to Field Bean Flowers (Vicia faba L.). The Journal of Applied Ecology 13: 749-752. https://doi.org/10.2307/2402252 DOI: https://doi.org/10.2307/2402252

King C, Ballantyne G, Willmer PG (2013) Why flower visitation is a poor proxy for pollination: measuring single-visit pollen deposition, with implications for pollination networks and conservation. Methods in Ecology and Evolution 4: 811-818. https://doi.org/10.1111/2041-210X.12074 DOI: https://doi.org/10.1111/2041-210X.12074

Klein AM, Steffan-Dewenter I, Tscharntke T (2003) Fruit set of highland coffee increases with the diversity of pollinating bees. Proceedings of the Royal Society B: Biological Sciences 270: 955-961. https://doi.org/10.1098/rspb.2002.2306 DOI: https://doi.org/10.1098/rspb.2002.2306

Klein AM, Vaissière E, Cane JH, Steffan-Dewenter I, Cunningham SA, Kremen C, TscharntkeT (2007) Importance of pollinators in changing landscapes for world crops. Proceedings of the Royal Society B: Biological Sciences 274: 303-313. https://doi.org/10.1098/rspb.2006.3721 DOI: https://doi.org/10.1098/rspb.2006.3721

Lavorel S, Garnier E (2002) Predicting changes in community composition and ecosystem functioning from plant traits: revisiting the Holy Grail. Functional Ecology 16: 545-556. https://doi.org/10.1046/j.1365-2435.2002.00664.x DOI: https://doi.org/10.1046/j.1365-2435.2002.00664.x

Lavorel S, Grigulis K, McIntyre S, Williams NSG, Garden D, Dorrough J, Dorrough J, Berman S, Quétier F, Thébault A, Bonis A (2008) Assessing functional diversity in the field - Methodology matters! Functional Ecology 22: 134-147. https://doi.org/10.1111/j.1365-2435.2007.01339.x DOI: https://doi.org/10.1111/j.1365-2435.2007.01339.x

Lloyd DG, Schoen DJ (1992) Self- and cross-fertilization in plants. I. Functional dimensions. International Journal of Plant Sciences 153: 358-369. https://doi.org/10.1086/297040 DOI: https://doi.org/10.1086/297040

Lonsdorf E, Kremen C, Ricketts T, Winfree R, Williams N, Greenleaf S (2009) Modelling pollination services across agricultural landscapes. Annals of Botany 103: 1589-1600. https://doi.org/10.1093/aob/mcp069 DOI: https://doi.org/10.1093/aob/mcp069

Luca PA De, Vallejo-Marín M (2013) What's the "buzz" about? The ecology and evolutionary significance of buzz-pollination. Current Opinion in Plant Biology 16: 429-435. https://doi.org/10.1016/j.pbi.2013.05.002 DOI: https://doi.org/10.1016/j.pbi.2013.05.002

Mallinger RE, Gratton C (2015) Species richness of wild bees, but not the use of managed honeybees, increases fruit set of a pollinator-dependent crop. Journal of Applied Ecology 52: 323-330. https://doi.org/10.1111/1365-2664.12377 DOI: https://doi.org/10.1111/1365-2664.12377

Mammola S, Carmona CP, Guillerme T, Cardoso P (2021) Concepts and applications in functional diversity. Functional Ecology 35: 1869-1885. https://doi.org/10.1111/1365-2435.13882 DOI: https://doi.org/10.1111/1365-2435.13882

Martins KT, Gonzalez A, Lechowicz MJ (2015) Pollination services are mediated by bee functional diversity and landscape context. Agriculture, Ecosystems and Environment 200: 12-20. https://doi.org/10.1016/j.agee.2014.10.018 DOI: https://doi.org/10.1016/j.agee.2014.10.018

Marzinzig B, Brünjes L, Biagioni S, Behling H, Link W, Westphal C (2018) Bee pollinators of faba bean (Vicia faba L.) differ in their foraging behaviour and pollination efficiency. Agriculture, Ecosystems and Environment 264: 24-33. https://doi.org/10.1016/j.agee.2018.05.003 DOI: https://doi.org/10.1016/j.agee.2018.05.003

Millard JW, Freeman R, Newbold T (2020) Text-analysis reveals taxonomic and geographic disparities in animal pollination literature. Ecography 43: 44-59. https://doi.org/10.1111/ecog.04532 DOI: https://doi.org/10.1111/ecog.04532

Mori AS, Furukawa T, Sasaki T (2013) Response diversity determines the resilience of ecosystems to environmental change. Biological Reviews 88: 349-364. https://doi.org/10.1111/brv.12004 DOI: https://doi.org/10.1111/brv.12004

Newton SD, Hill GD (1983) Robbing of Field Bean Flowers by the Short-Tongued Bumble Bee Bombus terrestris L. Journal of Apicultural Research 22: 124-129. https://doi.org/10.1080/00218839.1983.11100573 DOI: https://doi.org/10.1080/00218839.1983.11100573

Nuñez MA, Chiuffo MC, Pauchard A, Zenni RD (2021) Making ecology really global. Trends in Ecology, Evolution 36: 766-769. https://doi.org/10.1016/j.tree.2021.06.004 DOI: https://doi.org/10.1016/j.tree.2021.06.004

Ollerton J, Winfree R, Tarrant S (2011) How many flowering plants are pollinated by animals? Oikos 120: 321-326. https://doi.org/10.1111/j.1600-0706.2010.18644.x DOI: https://doi.org/10.1111/j.1600-0706.2010.18644.x

Orr MC, Hughes AC, Chesters D, Pickering J, Zhu C-D, Ascher JS (2021) Global patterns and drivers of bee distribution. Current Biology 31: 451-458.e4. https://doi.org/10.1016/j.cub.2020.10.053 DOI: https://doi.org/10.1016/j.cub.2020.10.053

Peat J, Goulson D (2005) Effects of experience and weather on foraging rate and pollen versus nectar collection in the bumblebee, Bombus terrestris. Behavioral Ecological Sociobiology 58: 152-156. https://doi.org/10.1007/s00265-005-0916-8 DOI: https://doi.org/10.1007/s00265-005-0916-8

Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE (2010) Global pollinator declines: trends, impacts and drivers. Trends in Ecology, Evolution 25: 345-353. https://doi.org/10.1016/j.tree.2010.01.007 DOI: https://doi.org/10.1016/j.tree.2010.01.007

Powney GD, Carvell C, Edwards M, Morris RKA, Roy HE, Woodcock BA, Isaac NJB (2019) Widespread losses of pollinating insects in Britain. Nature Communications 10: 1018. https://doi.org/10.1038/s41467-019-08974-9 DOI: https://doi.org/10.1038/s41467-019-08974-9

Rader R, Bartomeus I, Garibaldi LA, Garratt MPD, Howlett BG, Winfree R, Cunningham SA, Mayfield MM, Arthur AD, Andersson GKS, Bommarco R, Brittain C, Carvalheiro LG, Chacoff NP, Entling MH, Foully B, Freitas BM, Gemmill-Herren B, Ghazoul J, Griffin SR, Gross CL, Herbertsson L, Herzog F, Hipólito J, Jaggar S, Jauker F, Klein AM, Kleijn D, Krishnan S, Lemos CQ, Lindström SAM, Mandelik Y, Monteiro VM, Nelson W, Nilsson L, Pattemore DE, de O. Pereira N, Pisanty G, Potts SG, Reemer M, Rundlöf M, Sheffield CS, Scheper J, Schüepp C, Smith HG, Stanley DA, Stout JC, Szentgyörgyi H, Taki H, Vergara CH, Viana BF Woyciechowski, Michal (2016) Non-bee insects are important contributors to global crop pollination. Proceedings of the National Academy of Sciences 113: 146-151. https://doi.org/10.1073/pnas.1517092112 DOI: https://doi.org/10.1073/pnas.1517092112

Roches S Des, Post DM, Turley NE, Bailey JK, Hendry AP, Kinnison MT, et al. (2018) The ecological importance of intraspecific variation. Nature Ecology and Evolution 2: 57-64. https://doi.org/10.1038/s41559-017-0402-5 DOI: https://doi.org/10.1038/s41559-017-0402-5

Roquer-Beni L, Alins G, Arnan X, Boreux V, García D, Hambäck PA, Happe AK, Klein AM, Miñarro M, Mody K, Porcel M, Rodrigo A, Samnegård U, Tasin M, Bosch J (2021) Management-dependent effects of pollinator functional diversity on apple pollination services: A response-effect trait approach. Journal of Applied Ecology 10.1111/1365-2664.14022. https://doi.org/10.1111/1365-2664.14022 DOI: https://doi.org/10.1111/1365-2664.14022

Sahli HF, Conner JK (2006) Characterizing ecological generalization in plant-pollination systems. Oecologia 148: 365-372. https://doi.org/10.1007/s00442-006-0396-1 DOI: https://doi.org/10.1007/s00442-006-0396-1

Speight MC, Castella E, Sarthou J-P (2020) Syrph the Net. 12th edn. Syrph the Net Publications, Dublin.

Stavert JR, Liñán-Cembrano G, Beggs JR, Howlett BG, Pattemore DE, Bartomeus I (2016) Hairiness: The missing link between pollinators and pollination. PeerJ e2779. https://doi.org/10.7717/peerj.2779 DOI: https://doi.org/10.7717/peerj.2779

Suzuki K (1994). Pollinator restriction in the narrow-tube flower type of Mertensia ciliata (James) G. Don (Boraginaceae). Plant Species Biology 9: 69-73 https://doi.org/10.1111/j.1442-1984.1994.tb00085.x DOI: https://doi.org/10.1111/j.1442-1984.1994.tb00085.x

Thomson JD, Goodell K (2002) Pollen removal and deposition by honeybee and bumblebee visitors to apple and almond flowers. Journal of Applied Ecology 38: 1032-1044. https://doi.org/10.1046/j.1365-2664.2001.00657.x DOI: https://doi.org/10.1046/j.1365-2664.2001.00657.x

Vázquez DP, Morris WF, Jordano P (2005) Interaction frequency as a surrogate for the total effect of animal mutualists on plants. Ecology Letters 8: 1088-1094. https://doi.org/10.1111/j.1461-0248.2005.00810.x DOI: https://doi.org/10.1111/j.1461-0248.2005.00810.x

Warzecha D, Diekötter T, Wolters V, Jauker F (2016) Intraspecific body size increases with habitat fragmentation in wild bee pollinators. Landscape Ecology 31: 1449-1455. https://doi.org/10.1007/s10980-016-0349-y DOI: https://doi.org/10.1007/s10980-016-0349-y

Willmer P, Finlayson K. (2014) Big bees do a better job: intraspecific size variation influences pollination effectiveness. Journal of Pollination Ecology 14: 244-254. https://doi.org/10.26786/1920-7603(2014)22 DOI: https://doi.org/10.26786/1920-7603(2014)22

Winfree R, Fox JW, Williams NM, Reilly JR, Cariveau DP (2015) Abundance of common species, not species richness, drives delivery of a real-world ecosystem service. Ecology Letters 18: 626-635. https://doi.org/10.1111/ele.12424 DOI: https://doi.org/10.1111/ele.12424

Woodcock BA, Edwards M, Redhead J, Meek WR, Nuttall P, Falk S, Nowakowski M, Pywell RF (2013) Crop flower visitation by honeybees, bumblebees and solitary bees: small scale behavioural differences linked to landscape scale responses. Agriculture, Ecosystems, Environment, 171: 1-8. https://doi.org/10.1016/j.agee.2013.03.005 DOI: https://doi.org/10.1016/j.agee.2013.03.005

Woodcock BA, Garratt, MPD, Powney GD, Shaw RF, Osborne JL, Soroka J, Lindström SAM, Stanley D, Ouvrard P, Edwards ME, Jauker F, McCracken ME, Zou Y, Potts SG, Rundlöf M, Noriega JA, Greenop A, Smith HG, Bommarco R, van der Werf W, Stout JC, Steffan-Dewenter I, Morandin L, Bullock JM, Pywell RF (2019) Meta-analysis reveals that pollinator functional diversity and abundance enhance crop pollination and yield. Nature Communications, 10: 1481. https://doi.org/10.1038/s41467-019-09393-6 DOI: https://doi.org/10.1038/s41467-019-09393-6

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Published

2023-10-04

How to Cite

Greenop, A., Woodcock, B., & Pywell, R. F. . (2023). Using functional traits to predict pollination services: A review. Journal of Pollination Ecology, 35, 194–206. https://doi.org/10.26786/1920-7603(2023)735

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