Abstract
Biotic and abiotic factors may individually or interactively disrupt plant–pollinator interactions, influencing plant fitness. Although variations in temperature and precipitation are expected to modify the overall impact of predators on plant–pollinator interactions, few empirical studies have assessed if these weather conditions influence anti-predator behaviors and how this context-dependent response may cascade down to plant fitness. To answer this question, we manipulated predation risk (using artificial spiders) in different years to investigate how natural variation in temperature and precipitation may affect diversity (richness and composition) and behavioral (visitation) responses of flower-visiting insects to predation risk, and how these effects influence plant fitness. Our findings indicate that predation risk and an increase in precipitation independently reduced plant fitness (i.e., seed set) by decreasing flower visitation. Predation risk reduced pollinator visitation and richness, and altered species composition of pollinators. Additionally, an increase in precipitation was associated with lower flower visitation and pollinator richness but did not alter pollinator species composition. However, maximum daily temperature did not affect any component of the pollinator assemblage or plant fitness. Our results indicate that biotic and abiotic drivers have different impacts on pollinator behavior and diversity with consequences for plant fitness components. Even small variation in precipitation conditions promotes complex and substantial cascading effects on plants by affecting both pollinator communities and the outcome of plant–pollinator interactions. Tropical communities are expected to be highly susceptible to climatic changes, and these changes may have drastic consequences for biotic interactions in the tropics.
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References
Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol. https://doi.org/10.1111/j.1442-9993.2001.01070.pp.x
Antiqueira PAP (2012) Efeitos indiretos de predadores e de herbívoros florais no comportamento de visitantes florais e sucesso reprodutivo de Rubus rosifolius. Dissertação de mestrado, Universidade Estadual Paulista
Antiqueira PAP, Romero GQ (2016) Floral asymmetry and predation risk modify pollinator behavior, but only predation risk decreases plant fitness. Oecologia 181:475–485. https://doi.org/10.1007/s00442-016-3564-y
Armbruster WS, McCormick KD (1990) Diel foraging patterns of male euglossine bees: ecological causes and evolutionary response by plants. Biotropica 22:160–171. https://doi.org/10.2307/2388409
Bale JS, Masters GJ, Hodkinson ID, Awmack C et al (2002) Herbivory in global climate change research: direct effects of rising temperature on insect herbivores. Glob Change Biol 8:1–16. https://doi.org/10.1046/j.1365-2486.2002.00451.x
Bartomeus I, Ascher JS, Wagner D, Danforth BN, Colla S, Kornbluth S, Winfree R (2011) Climate-associated phenological advances in bee pollinators and bee-pollinated plants. Proc Natl Acad Sci 108:20645–20649. https://doi.org/10.1073/pnas.1115559108
Barton BT (2010) Climate warming and predation risk during herbivore ontogeny. Ecology 10:2811–2818. https://doi.org/10.1890/09-2278.1
Barton BT, Schmitz OJ (2009) Experimental warming transforms multiple predator effects in a grassland food web. Ecol Lett 12:1317–1352. https://doi.org/10.1111/j.1461-0248.2009.01386.x
Battisti A, Stastny M, Netherer S, Robinet S, Schopf A, Roques A, Larsson S (2005) Expansion of geographic range in the pine processionary moth caused by increased winter temperatures. Ecol Appl 15:2084–2096. https://doi.org/10.1890/04-1903
Bellard C, Bertelsmeier C, Leadley P, Thuiller W (2012) Impacts of climate change on the future of biodiversity. Ecol Lett 15:365–377. https://doi.org/10.1111/j.1461-0248.2011.01736.x
Brechbühl R, Casas J, Bacher S (2010) Ineffective crypsis in a crab spider: a prey community perspective. Proc R Soc B 277:739–746. https://doi.org/10.1098/rspb.2009.1632
Burkle LA, Marlin JC, Knight TM (2013) Plant–pollinator interaction over 120 years: loss of species, co-occurrence, and function. Science 339:1611–1615. https://doi.org/10.1126/science.1232728
Chamberlain SA, Bronstein JL, Rudgers JA (2014) How context dependent are species interactions? Ecol Lett 17:881–890. https://doi.org/10.1111/ele.12279
Chambers LE, Altwegg R, Barbraud C, Barnard P, Beaumont L, Crawford RJM, Durant JM et al (2013) Phenological changes in the Southern Hemisphere. PLoS One 8:e75514. https://doi.org/10.1371/journal.pone.0075514
Chappel MA (1984) Temperature regulation and energetics of the solitary bee Centris pallida during foraging and intermale mate competition. Physiol Zool 57:215–225. https://doi.org/10.1086/physzool.57.2.30163707
Corbet SA, Fussel M, Ake R, Fraser A, Gunson C, Savage A, Smith K (1993) Temperature and the pollinating activity of social bees. Ecol Entomol 18:17–30. https://doi.org/10.1111/j.1365-2311.1993.tb01075.x
Deutsch CA, Tewksbury JJ, Huey RB, Sheldon KS, Ghalambor CK, Haak DC (2008) Impacts of climate warming on terrestrial ectotherms across latitude. Proc Natl Acad Sci 105:6668–6672. https://doi.org/10.1073/pnas.0709472105
Devoto M, Medan D, Roig-Alsina A, Montaldo NH (2009) Patterns of species turnover in plant–pollinator communities along a precipitation gradient in Patagonia (Argentina). Austral Ecol 34:848–857. https://doi.org/10.1111/j.1442-9993.2009.01987.x
Dossena M, Yvon-Durocher G, Grey J, Montoya JM, Perkins DM, Trimmer M, Woodward G (2012) Warming alters community size structure and ecosystem functioning. Proc R Soc B 279:3011–3019. https://doi.org/10.1098/rspb.2012.0394
Dukas R (2001) Effects of perceived danger on flower choice by bees. Ecol Lett 4:27–333. https://doi.org/10.1046/j.1461-0248.2001.00228.x
Dukas R (2005) Bumble bee predators reduce pollinator density and plant fitness. Ecology 86:1401–1406. https://doi.org/10.1890/04-1663
Dukas R, Morse DH (2005) Crab spiders show mixed effects on flower-visiting bees and no effect on plant fitness components. Ecoscience 12:244–247. https://doi.org/10.2980/i1195-6860-12-2-244.1
Forrest JRK (2015) Plant—pollinator interactions and phenological change: what can we learn about climate impacts from experiments and observations? Oikos 124:4–13. https://doi.org/10.1111/oik.01386
Gonçalves-Souza T, Omena PM, Souza JC, Romero GQ (2008) Trait-mediated effects on flowers: artificial spiders deceive pollinators and decrease plant fitness. Ecology 89:2407–2413. https://doi.org/10.1890/07-1881.1
Harley CDG (2011) Climate change, keystone predation, and biodiversity loss. Science 334:1124–1127. https://doi.org/10.1126/science.1210199
Hatfield JL, Prueger JH (2015) Temperature extremes: effect on plant growth and development. Weather Clim Extremes 10:4–10. https://doi.org/10.1016/j.wace.2015.08.001
Hegland SJ, Nielsen A, Lázaro A, Bjerknes A-L, Totland O (2009) How does climate warming affect plant–pollinator interactions? Ecol Lett. https://doi.org/10.1111/j.1461-0248.2008.01269.x
Herrera CM, Medrano M (2017) Pollination consequences of simulated intrafloral microbial warming in an early-blooming herb. Flora 232:142–149. https://doi.org/10.1016/j.flora.2016.10.003
Hooper DU, Chapin FS III, Ewel JJ et al (2005) Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol Monogr 75:3–35. https://doi.org/10.1890/04-0922
Ings TC, Chittka L (2009) Predator crypsis enhances behaviourally-mediated indirect effects on plants by altering bumblebee foraging preferences. Proc R Soc B 276:2031–2036. https://doi.org/10.1098/rspb.2008.1748
Janzen DH (1967) Why mountain passes are higher in the tropics. Am Nat 101:233–249. https://doi.org/10.1086/282487
Joern A, Danner BJ, Logan JD (2006) Natural history of mass-action in predator-prey models: a case study from wolf spiders and grasshoppers. Am Midl Nat 156:52–64. https://doi.org/10.1674/0003-0031(2006)156%5b52:NHOMIP%5d2.0.CO;2
Jones EI (2009) Optimal foraging when predation risk increases with patch resources: an analysis of pollinators and ambush predators. Oikos 119:835–840. https://doi.org/10.1111/j.1600-0706.2009.17841.x
Jones EI, Dornhaus A (2011) Predation risk makes bees reject rewarding flowers and reduce foraging activity. Behav Ecol Sociobiol 65:1505–1511. https://doi.org/10.1007/s00265-011-1160-z
Kersch-Becker MF, Grisolia BB, Campos MJO, Romero GQ (2017) Community-wide responses to predation risk: effects of predator hunting mode on herbivores, pollinators and parasitoids. Ecol Entomol 43:846–849. https://doi.org/10.1111/een.12660
Kersch-Becker MF, Grisolia BB, Campos MJ, Romero GQ (2018) The role of spider hunting mode on the strength of spider–plant mutualisms. Oecologia 188:231-222. https://doi.org/10.1007/s00442-018-4170-y
Kevan PG (1975) Sun-tracking solar furnaces in high arctic flowers: significance for pollination and insects. Science 189:723–726. https://doi.org/10.1126/science.189.4204.723
Kudo G, Ida TY (2013) Early onset of spring increases the phenological mismatch between plants and pollinators. Ecology 94:2311–2320. https://doi.org/10.1890/12-2003.1
Kudo G, Nishikawa T, Kasagi T, Kosuge S (2004) Does seed production of spring ephemerals decrease when spring comes early? Ecol Res 19:255–259. https://doi.org/10.1111/j.1440-1703.2003.00630.x
Laws AN (2017) Climate change effects on predator–prey interactions. Curr Opin Insect 406(23):28–34. https://doi.org/10.1016/j.cois.2017.06.010
Lawson DA, Rands SA (2019) The effects of rainfall on plant–pollinator interactions. Arthropod-Plant Interactions 13:561–569. https://doi.org/10.1007/s11829-019-09686-z
Lefcheck JS (2016) PiecewiseSEM: piecewise structural equation modeling in R for ecology, evolution, and systematics. Methods Ecol Evol 7:573–579. https://doi.org/10.1111/2041-210X.12512
Leitão-Filho HDF (1992) A flora arbórea da Serra do Japi. História natural da Serra do Japi: Ecologia e preservação de uma área florestal no sudeste do Brasil. Unicamp/Fapesp
Loreau M, Naeem S, Inchausti P, Bengtsson J, Grime JP, Hector A, Hooper DU, Huston MA, Raffaelli D, Schmid B, Tilman D, Wardle DA (2001) Biodiversity and ecosystem functioning: current knowledge and future challenges. Science 294:804–808. https://doi.org/10.1126/science.1064088
Morse DH (2007) Predator upon a flower: life history and fitness in a crab spider. Harvard University
Nicolson S, Human H (2013) Chemical composition of the ‘low quality’ pollen of sunflower (Helianthus annuus, Asteraceae). Apidologie 44:144–152. https://doi.org/10.1007/s13592-012-0166-5
Norgate M, Boyd-Gerny S, Simonov V, Rosa MGP, Heard TA, Dyer AG (2010) Ambient temperature influences Australian native stingless bee (Trigona carbonaria) preference for warm nectar. PLoS One 5:e12000. https://doi.org/10.1371/journal.pone.0012000
Ockendon N, Baker DJ, Carr JA et al (2014) Mechanisms underpinning climatic impacts on natural populations: altered species interactions are more important than direct effects. Glob Change Biol 20:2221–2229. https://doi.org/10.1111/gcb.12559
Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D et al (2018) Vegan: community Ecology Package. R package version 2(5-2):2018
Peat J, Goulson D (2005) Effects of experience and weather on foraging rate and pollen versus nectar collection in the bumblebee. Bombus terrestris. Behav Ecol Sociobiol 58(2):152–156. https://doi.org/10.1007/s00265-005-0916-8
Pellissier L, Albouy C, Bascompte J et al (2017) Comparing species interaction networks along environmental gradients. Biol Rev 93:785–800. https://doi.org/10.1111/brv.12366
Pereboom JJ, Biesmeijer JC (2003) Thermal constraints for stingless bee foragers: the importance of body size and coloration. Oecologia 137:42–50. https://doi.org/10.1111/brv.12366
Pinheiro JC, Bates DM (2000) Mixed effects models in S and S-Plus. Springer, New York
Polatto LP, Chaud-Neto J, Alves-Junior VV (2014) Influnce of abiotic factors and floral resource availability on daily foraging activity of bees. J Insect Beha 27:593–612. https://doi.org/10.1007/s10905-014-9452-6
R Core Team (2018) R: A language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. www.R-project.org
Rands SA, Whitney AM (2008) Floral temperature and optimal foraging: is heat a feasible floral reward for pollinators? PLoS One 3:e269. https://doi.org/10.1371/journal.pone.0002007
Reader T, Higginson AD, Barnard CJ, Gilbert FS (2006) The effects of predation risk from crab spiders on bee foraging behavior. Behav Ecol 16:933–939. https://doi.org/10.1093/beheco/arl027
Romero GQ, Antiqueira PA, Koricheva J (2011) A meta-analysis of predation risk effects on pollinator behavior. PLoS One 6:e20689. https://doi.org/10.1371/journal.pone.0020689
Romero GQ, Gonçalves-Souza T, Kratina P, Marino NA, Petry WK, Sobral-Souza T, Roslin T (2018) Global predation pressure redistribution under future climate change. Nat Clim Change 8:1087. https://doi.org/10.1038/s41558-018-0347-y
Sanderson RA, Goffe LA, Leifert C (2015) Time-series models to quantify short- term effects of meteorological conditions on bumblebee forager activity in agricultural landscapes. Agric For Entomol 17:270–276. https://doi.org/10.1111/afe.12102
Scaven VL, Rafferty NE (2013) Physiological effects of climate warming on flowering plants and insect pollinators and potential consequences for their interactions. Curr Zool 59:418–426. https://doi.org/10.1093/czoolo/59.3.418
Schweiger O, Biesmeijer JC, Bommarco R, Hickler T, Hulme PE, Klotz S et al (2010) Multiple stressors on biotic interactions: how climate change and alien species interact to affect pollination. Biol Rev 85:777–795. https://doi.org/10.1111/j.1469-185X.2010.00125.x
Sheldon KS, Huey RB, Kaspari M, Sanders NJ (2018) Fifty years of mountain passes: a perspective on Dan Janzen’s classic article. Am Nat 191:553–565. https://doi.org/10.1086/697046
Stankowich T, Blumstein DT (2005) Fear in animals: a meta-analysis and review of risk assessment. Proc R Soc B 272:2627–2634. https://doi.org/10.1098/rspb.2005.3251
Tylianakis JM, Didham RK, Bascompte J, Wardle DA (2008) Global change and species interactions in terrestrial ecosystems. Ecol Lett 11:1351–1363. https://doi.org/10.1111/j.1461-0248.2008.01250.x
van der Kooi CJ, Kevan PG, Koski MH (2019) The thermal ecology of flowers. Ann Bot 20:1–11. https://doi.org/10.1093/aob/mcz073
van der Putten WH, Macel M, Visser ME (2010) Predicting species distribution and abundance responses to climate change: why it is essential to include biotic interactions across trophic levels. Phil Trans R Soc B 365:2025–2034. https://doi.org/10.1098/rstb.2010.0037
Vicens N, Bosch J (2000) Weather-dependent pollinator activity in an apple orchard, with special reference to Osmia cornuta and Apis mellifera (Hymenoptera: Megachilidae and Apidae). Environ Entomol 29:413–420. https://doi.org/10.1603/0046-225X-29.3.413
Whitney HM, Dyer A, Chittka L, Rands SA, Glover BJ (2008) The interaction of temperature and sucrose concentration on foraging preferences in bumblebees. Naturwissenschaften 95:845–850. https://doi.org/10.1007/s00114-008-0393-9
Zuur A, Ieno EN, Walker N, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer Science & Business Media. https://doi.org/10.1007/978-0-387-87458-6
Acknowledgements
We would like to thank the staff in the City Hall of Jundiaí, the Biological Reserve of Serra do Japi, Jundiaí; the Integrated Center for Agrometeorological Information (CIIAGRO) and Dr. Angelica Prela Pantano for providing the weather dataset from the study site; Mark P. Nessel for the suggestions on the early versions of the manuscript. Finally, we are grateful to the Handling Editor, Dr. Jessica Forrest and two anonymous reviewers for comments and suggestions which have improved the quality of the manuscript. P. A. P. Antiqueira received a postdoc scholarship from the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP; proc. no. 2017/26243-8). G. Q. Romero received a productivity grant from the Brazilian National Council for Scientific and Technological Development (Conselho Nacional de Desenvolvimento Científico e Tecnológico). P. M de Omena was supported by “Coordenação de Aperfeiçoamento Pessoal de Nível Superior (PNPD-CAPES; 2014/0603-4). C. Vieira was supported by Fundação de Apoio à Pesquisa do Estado de São Paulo/FAPESP (2010/51523-5). The present study was funded by FAPESP.
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PAPA and GQR conceptualized the research; PAPA, TGS and PMO conducted the experiments and collected the data; PAPA and TGS analyzed the data; PAPA, CV, FCR, GHM, MFKB, PMO, SBG, TGS, TNB and GQR wrote the manuscript.
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Communicated by Jessica Forrest.
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Antiqueira, P.A.P., de Omena, P.M., Gonçalves-Souza, T. et al. Precipitation and predation risk alter the diversity and behavior of pollinators and reduce plant fitness. Oecologia 192, 745–753 (2020). https://doi.org/10.1007/s00442-020-04612-0
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DOI: https://doi.org/10.1007/s00442-020-04612-0