Abstract
Growing evidence of global declines in pollinator abundance and diversity has raised concerns about the resilience of pollination systems. When subjected to stressors, each nested component of the pollination system (communities, populations, and colonies) can respond in either a smooth linear fashion, or in an abrupt nonlinear manner. Threshold and tipping point responses to stress are of particular concern because they result in sudden changes with little warning; such changes may lead to persistent non-functional states that are difficult to reverse. Here, we review evidence for threshold and tipping point responses at the colony, population and community levels of the pollination system. We find that while there are strong theoretical reasons to expect tipping point and threshold responses at all three levels of the pollination system, evidence in the field is lacking for all levels except the colony level. While this is encouraging, caution is still warranted as tipping point and threshold responses—by their very nature—may not be apparent until they are underway. Moreover, we propose that the interaction of nonlinear stress responses across different levels of the pollination system can increase the risk of cascading failures. We therefore suggest a cautious approach toward the management of pollination systems. Since environmental change will almost certainly continue to accelerate, understanding the potential for thresholds, tipping points and cascading failures is key to safeguarding global pollination systems.
Similar content being viewed by others
References
Aizen MA, Morales CL, Morales JM (2008) Invasive mutualists erode native pollination webs. PLoS Biol 6(2):31
Aizen MA, Sabatino M, Tylianakis JM (2012) Specialization and rarity predict nonrandom loss of interactions from mutualist networks. Science 335:1486–1489
Allee WC, Park O, Emerson AE, Park T, Schmidt KP (1949) Principles of animal ecology. WB Saundere Co., Ltd
Barron AB (2015) Death of the bee hive: understanding the failure of an insect society. Curr Opin Insect Sci 10:45–50
Bartomeus I, Vilà M, Santamaría L (2008) Contrasting effects of invasive plants in plant–pollinator networks. Oecologia 155(4):761–770
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. Proc Nat Acad Sci 110(12):4656–4660
Bascompte J, Jordano P (2007) Plant-animal mutualistic networks: the architecture of biodiversity. Annu Rev Ecol Evol Syst 38:567–593
Bascompte J, Jordano P, Melián CJ, Olesen JM (2003) The nested assembly of plant–animal mutualistic networks. Proc Natl Acad Sci 100:9383–9387
Bastolla U, Fortuna MA, Pascual-García A, Ferrera A, Luque B, Bascompte J (2009) The architecture of mutualistic networks minimizes competition and increases biodiversity. Nature 458(7241):1018–1021
Bauch CT, Sigdel R, Pharaon J, Anand M (2016) Early warning signals of regime shifts in coupled human–environment systems. Proc Natl Acad Sci 113(51):14560–14567
Berec L, Angulo E, Courchamp F (2007) Multiple Allee effects and population management. Trends Ecol Evol 22:185–191
Biesmeijer JC, Roberts SP, Reemer M, Ohlemüller R, Edwards M, Peeters T, Thomas C, Settele J (2006) Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 313(5785):351–354
Boff S, Soro A, Paxton RJ, Alves-dos-Santos I (2014) Island isolation reduces genetic diversity and connectivity but does not significantly elevate diploid male production in a neotropical orchid bee. Conserv Genet 15:1123–1135
Bryden J, Gill RJ, Mitton RA, Raine NE, Jansen VA (2013) Chronic sublethal stress causes bee colony failure. Ecol Lett 16:1463–1469
Burden CM, Elmore C, Hladun KR, Trumble JT, Smith BH (2016) Acute exposure to selenium disrupts associative conditioning and long-term memory recall in honey bees (Apis mellifera). Ecotoxicol Environ Saf 127:71–79
Burkle LA, Marlin JC, Knight TM (2013) Plant-pollinator interactions over 120 years: loss of species, co-occurrence, and function. Science 339:1611–1615
Calabrese JM, Fagan WF (2004) Lost in time, lonely, and single: reproductive asynchrony and the Allee effect. Am Nat 164:25–37
Carpenter SR, Cole JJ, Pace ML, Batt R, Brock W, Cline T, Coloso J, Hodgson JR, Kitchell JF, Seekell DA (2011) Early warnings of regime shifts: a whole-ecosystem experiment. Science 332:1079–1082
Carvalheiro LG, Kunin WE, Keil P, Aguirre-Gutiérrez J, Ellis WN, Fox R, Groom Q, Hennekens S, Van Landuyt W, Maes D (2013) Species richness declines and biotic homogenisation have slowed down for NW-European pollinators and plants. Ecol Lett 16(7):870–878
Chapman RE, Bourke AF (2001) The influence of sociality on the conservation biology of social insects. Ecol Lett 4:650–662
Courchamp F, Clutton-Brock T, Grenfell B (1999) Inverse density dependence and the Allee effect. Trends Ecol Evol 14:405–410
Dai L, Vorselen D, Korolev KS, Gore J (2012) Generic indicators for loss of resilience before a tipping point leading to population collapse. Science 336:1175–1177
Dakos V, Bascompte J (2014) Critical slowing down as early warning for the onset of collapse in mutualistic communities. Proc Natl Acad Sci 111:17546–17551
Dakos V, Carpenter SR, Brock WA, Ellison AM, Guttal V, Ives AR, Kéfi S, Livina V, Seekell DA, van Nes EH (2012) Methods for detecting early warnings of critical transitions in time series illustrated using simulated ecological data. PLoS ONE 7:e41010
Darvill B, Lepais O, Woodall L, Goulson D (2012) Triploid bumblebees indicate a direct cost of inbreeding in fragmented populations. Mol Ecol 21:3988–3995
De Palma A, Kuhlmann M, Roberts SP, Potts SG, Börger L, Hudson LN, Lysenko I, Newbold T, Purvis A (2015) Ecological traits affect the sensitivity of bees to land-use pressures in European agricultural landscapes. J Appl Ecol 52:1567–1577
Elias J, Dorn S, Mazzi D (2010) No evidence for increased extinction proneness with decreasing effective population size in a parasitoid with complementary sex determination and fertile diploid males. BMC Evol Biol 10(1):366. https://doi.org/10.1186/1471-2148-10-366
Fagan WF, Holmes E (2006) Quantifying the extinction vortex. Ecol Lett 9:51–60
Faria LRR, Soares EDG, Carmo ED, Oliveira PMCD (2016) Diploid male dynamics under different numbers of sexual alleles and male dispersal abilities. Theory Biosci 135:111–119
Foley MM, Martone RG, Fox MD, Kappel CV, Mease LA, Erickson AL, Halpern BS, Selkoe KA, Taylor P, Scarborough C (2015) Using ecological thresholds to inform resource management: current options and future possibilities. Front Mar Sci 2:95
Gallai N, Salles JM, Settele J, Vaissière BE (2009) Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecol Econ 68(3):810–821
Gegear RJ, Otterstatter MC, Thomson JD (2006) Bumble-bee foragers infected by a gut parasite have an impaired ability to utilize floral information. Proc R Soc Lond B 273:1073–1078
Geslin B, Gauzens B, Baude M, Dajoz I, Fontaine C, Henry M, Ropars L, Rollin O, Thébault E, Vereecken NJ (2017) Massively introduced managed species and their consequences for plant–pollinator interactions. In Advances in ecological research, vol 57. Academic Press, pp 147–199
Gilpin M (1986) Minimum viable populations: processes of extinction. In: Soulé ME (ed) Conservation biology: the science of scarcity and diversity. Sinauer Associates, Sunderland
Gloag R, Ding G, Christie JR, Buchmann G, Beekman M, Oldroyd BP (2016) An invasive social insect overcomes genetic load at the sex locus. Nat Ecol Evol 1:0011
González-Varo JP, Biesmeijer JC, Bommarco R, Potts SG, Schweiger O, Smith HG, Steffan-Dewenter I, Szentgyörgyi H, Woyciechowski M, Vilà M (2013) Combined effects of global change pressures on animal-mediated pollination. Trends Ecol Evol 28(9):524–530
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
Greenleaf SS, Williams NM, Winfree R, Kremen C (2007) Bee foraging ranges and their relationship to body size. Oecologia 153:589–596
Grilli J, Rogers T, Allesina S (2016) Modularity and stability in ecological communities. Nat Commun 7:2031
Gsell AS, Scharfenberger U, Özkundakci D, Walters A, Hansson L-A, Janssen ABG, Nõges P, Reid PC, Schindler DE, Van Donk E, Dakos V, Adrian R (2016) Evaluating early-warning indicators of critical transitions in natural aquatic ecosystems. Proc Natl Acad Sci 113(50):E8089–E8095
Hedrick PW, Gadau J, Page RE (2006) Genetic sex determination and extinction. Trends Ecol Evol 21:55–57
Hein S, Poethke H-J, Dorn S (2009) What stops the ‘diploid male vortex’?—A simulation study for species with single locus complementary sex determination. Ecol Model 220:1663–1669
Henry M, Becher MA, Osborne JL, Kennedy PJ, Aupinel P, Bretagnolle V, Brun F, Grimm V, Horn J, Requier F (2017) Predictive systems models can help elucidate bee declines driven by multiple combined stressors. Apidologie 48(3):328–339
Huang Z-Y, Robinson GE (1996) Regulation of honey bee division of labor by colony age demography. Behav Ecol Sociobiol 39:147–158
Hughes TP, Linares C, Dakos V, van de Leemput IA, van Nes EH (2013) Living dangerously on borrowed time during slow, unrecognized regime shifts. Trends Ecol Evol 28:149–155
Hunsicker ME, Kappel CV, Selkoe KA, Halpern BS, Scarborough C, Mease L, Amrhein A (2016) Characterizing driver–response relationships in marine pelagic ecosystems for improved ocean management. Ecol Appl 26:651–663
Jiang J, Huang ZG, Seager TP, Lin W, Grebogi C, Hastings A, Lai YC (2018) Predicting tipping points in mutualistic networks through dimension reduction. Proc Nat Acad Sci 115(4):E639–E647
Jin N, Klein S, Leimig F, Bischoff G, Menzel R (2015) The neonicotinoid clothianidin interferes with navigation of the solitary bee Osmia cornuta in a laboratory test. J Exp Biol 218:2821–2825
Kaiser-Bunbury CN, Muff S, Memmott J, Müller CB, Caflisch A (2010) The robustness of pollination networks to the loss of species and interactions: a quantitative approach incorporating pollinator behaviour. Ecol Lett 13:442–452
Kéfi S, Dakos V, Scheffer M, Van Nes EH, Rietkerk M (2013) Early warning signals also precede non-catastrophic transitions. Oikos 122:641–648
Kelly RP, Erickson AL, Mease LA, Battista W, Kittinger JN, Fujita R (2015) Embracing thresholds for better environmental management. Philos Trans R Soc Lond B 370:20130276
Khoury DS, Myerscough MR, Barron AB (2011) A quantitative model of honey bee colony population dynamics. PLoS ONE 6:e18491
Klein A-M, Vaissiere BE, Cane JH, Steffan-Dewenter I, Cunningham SA, Kremen C, Tscharntke T (2007) Importance of pollinators in changing landscapes for world crops. Proc R Soc B 274:303–313
Klein S, Cabirol A, Devaud J-M, Barron AB, Lihoreau M (2017) Why bees are so vulnerable to environmental stressors. Trends Ecol Evol 32:268–278
Kramer AM, Dennis B, Liebhold AM, Drake JM (2009) The evidence for Allee effects. Popul Ecol 51:341
Leonard RJ, Hochuli DF (2017) Exhausting all avenues: why impacts of air pollution should be part of road ecology. Front Ecol Environ 15(8):443–449
Lever JJ, Nes EH, Scheffer M, Bascompte J (2014) The sudden collapse of pollinator communities. Ecol Lett 17:350–359
Levin SA (1998) Ecosystems and the biosphere as complex adaptive systems. Ecosystems 1(5):431–436
Memmott J, Waser NM, Price MV (2004) Tolerance of pollination networks to species extinctions. Proc R Soc Lond B 271:2605–2611
Memmott J, Craze PG, Waser NM, Price MV (2007) Global warming and the disruption of plant–pollinator interactions. Ecol Lett 10(8):710–717
Myerscough MR, Khoury DS, Ronzani S, Barron AB (2017) Why do hives die? Using mathematics to solve the problem of honey bee colony collapse. The role and importance of mathematics in innovation. Springer, Berlin, pp 35–50
Olesen JM, Bascompte J, Dupont YL, Jordano P (2007) The modularity of pollination networks. Proc Natl Acad Sci 104:19891–19896
Ollerton J, Winfree R, Tarrant S (2011) How many flowering plants are pollinated by animals? Oikos 120:321–326
Pascual M, Dunne JA (eds) (2006) Ecological networks: linking structure to dynamics in food webs. Oxford University Press, Oxford
Perry CJ, Søvik E, Myerscough MR, Barron AB (2015) Rapid behavioral maturation accelerates failure of stressed honey bee colonies. Proc Natl Acad Sci 112:3427–3432
Petanidou T, Kallimanis AS, Tzanopoulos J, Sgardelis SP, Pantis JD (2008) Long-term observation of a pollination network: fluctuation in species and interactions, relative invariance of network structure and implications for estimates of specialization. Ecol Lett 11:564–575
Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE (2010) Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol 25(6):345–353
Rader R, Bartomeus I, Garibaldi LA, Garratt MP, Howlett BG, Winfree R, Cunningham SA, Mayfield MM, Arthur AD, Andersson GK, Bommarco R (2016) Non-bee insects are important contributors to global crop pollination. Proc Natl Acad Sci 113(1):146–151
Rafferty NE, CaraDonna PJ, Burkle LA, Iler AM, Bronstein JL (2013) Phenological overlap of interacting species in a changing climate: an assessment of available approaches. Ecol Evol 3(9):3183–3193
Revilla TA, Encinas-Viso F, Loreau M (2015) Robustness of mutualistic networks under phenological change and habitat destruction. Oikos 124:22–32
Richter A, Dakos V (2015) Profit fluctuations signal eroding resilience of natural resources. Ecol Econ 117:12–21
Robinson GE (1992) Regulation of division of labor in insect societies. Annu Rev Entomol 37:637–665
Sánchez-Bayo F, Wyckhuys KAG (2019) Worldwide decline of the entomofauna: a review of its drivers. Biol Cons 232:8–27
Saavedra S, Rohr RP, Dakos V, Bascompte J (2013) Estimating the tolerance of species to the effects of global environmental change. Nat Commun 4:2350
Scheffer M, Carpenter SR (2003) Catastrophic regime shifts in ecosystems: linking theory to observation. Trends Ecol Evol 18:648–656
Scheffer M, Carpenter S, Foley JA, Folke C, Walker B (2001) Catastrophic shifts in ecosystems. Nature 413:591–596
Scheffer M, Bascompte J, Brock WA, Brovkin V, Carpenter SR, Dakos V, Held H, van Nes EH, Rietkerk M, Sugihara G (2009) Early-warning signals for critical transitions. Nature 461:53–59
Schröder A, Persson L, De Roos AM (2005) Direct experimental evidence for alternative stable states: a review. Oikos 110:3–19
Stouffer DB, Cirtwill AR, Bascompte J (2014) How exotic plants integrate into pollination networks. J Ecol 102(6):1442–1450
Straub L, Williams GR, Pettis J, Fries I, Neumann P (2015) Superorganism resilience: eusociality and susceptibility of ecosystem service providing insects to stressors. Curr Opin Insect Sci 12:109–112
Tautz J, Maier S, Groh C, Rössler W, Brockmann A (2003) Behavioral performance in adult honey bees is influenced by the temperature experienced during their pupal development. Proc Natl Acad Sci 100:7343–7347
Timóteo S, Ramos JA, Vaughan IP, Memmott J (2016) High resilience of seed dispersal webs highlighted by the experimental removal of the dominant disperser. Curr Biol 26(7):910–915
Tylianakis JM, Morris RJ (2017) Ecological networks across environmental gradients. Annu Rev Ecol Evol Syst 48:25–48
Valdovinos FS, Moisset de Espanés P, Flores JD, Ramos-Jiliberto R (2013) Adaptive foraging allows the maintenance of biodiversity of pollination networks. Oikos 122:907–917
Van Wilgenburg E, Driessen G, Beukeboom LW (2006) Single locus complementary sex determination in Hymenoptera: an” unintelligent” design? Front Zool 3:1
Vanbergen AJ (2013) Threats to an ecosystem service: pressures on pollinators. Front Ecol Environ 11:251–259
Veraart AJ, Faassen EJ, Dakos V, van Nes EH, Lurling M, Scheffer M (2012) Recovery rates reflect distance to a tipping point in a living system. Nature 481:357–359
Whitehorn PR, Tinsley MC, Brown MJ, Darvill B, Goulson D (2009) Impacts of inbreeding on bumblebee colony fitness under field conditions. BMC Evol Biol 9:152
Williams NM, Crone EE, Roulston TAH, Minckley RL, Packer L, Potts SG (2010) Ecological and life-history traits predict bee species responses to environmental disturbances. Biol Conserv 143:2280–2291
Winfree R, Aguilar R, Vázquez DP, LeBuhn G, Aizen MA (2009) A meta-analysis of bees’ responses to anthropogenic disturbance. Ecology 90:2068–2076
Wissel C (1984) A universal law of the characteristic return time near thresholds. Oecologia 65(1):101–107
Yletyinen J, Brown P, Pech R, Hodges D, Hulme PE, Malcolm TF, Maseyk FJ, Peltzer DA, Perry GL, Richardson SJ, Smaill SJ (2019) Understanding and managing social-ecological tipping points in primary industries. Bioscience 69(5):335–347
Zayed A, Packer L (2005) Complementary sex determination substantially increases extinction proneness of haplodiploid populations. Proc Natl Acad Sci USA 102:10742–10746
Acknowledgements
The authors would like to thank Ignacio Bartomeus for his valuable comments and suggestions. We would also like to thank Johanna Yletyinen for kindly providing an early copy of her manuscript. Neither author declares a conflict of interest.
Funding
Funding were provided by Australian research council Discovery program (Grant No. DP190101994) and The Branco Weiss Fellowship – Society in Science.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Raphael K. Didham.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Glossary
- Allee effect
-
Allee effects occur when populations suffer from low or negative population growth when their population size is small
- Alternative stable states
-
Different states of a system that can occur under the same external conditions
- Bistability
-
The presence of two alternative stable states under the same conditions
- Extinction vortex
-
A self-reinforcing process that drives population size downward to extinction
- Hysteresis
-
The lack of reversibility in bistable systems; hysteresis refers to the phenomenon where the pathway to system degradation may not be the same as the pathway to restoration
- Threshold response
-
A strong nonlinear response of a system to small changes in environmental conditions or stressors
- Pollination system
-
Community composed of interacting pollinators (animals) and plants
- Positive feedback
-
A self-amplifying process between two or more system components
- Resilience indicators
-
Indicators of increasing instability in system dynamics that are used to detect proximity to tipping points (also referred to as early-warning signals)
- Tipping point
-
A point where a runaway process (usually due to a positive feedback) pushes a system to flip into a different state
Rights and permissions
About this article
Cite this article
Latty, T., Dakos, V. The risk of threshold responses, tipping points, and cascading failures in pollination systems. Biodivers Conserv 28, 3389–3406 (2019). https://doi.org/10.1007/s10531-019-01844-2
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10531-019-01844-2