Abstract
The significance of ecological non-monotonicity (a function whose first derivative changes signs) in sha** the structure and functions of the ecosystem has recently been recognized, but such studies involving high-order interactions are rare. Here, we have proposed a three-trophic conceptual diagram on interactions among trees, rodents, and insects in mast and non-mast years and tested the hypothesis that oak (Quercus wutaishanica) masting could result in increased mutualism and less predation in an oak-weevil-rodent system in a warm temperate forest of China. Our 14-year dataset revealed that mast years coincided with a relatively low rodent abundance but a high weevil abundance. Masting not only benefited seedling recruitment of oaks through increased dispersal by rodents but also a decrease in predation by rodents and weevils, as well as an increase in the overwintering survival of rodents. Masting appeared to have increased weevil survival by reducing predation of infested acorns by rodents. These results suggest that masting benefits all participants in the plant-insect-rodent system by increasing mutualism and reducing predation behavior (i.e., a non-monotonic function). Our study highlights the significance of masting in maintaining the diversity and function of the forest ecosystem by facilitating the transformation from predation to mutualism among trophic species.
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References
Bajocco, S., Ferrara, C., Bascietto, M., Alivernini, A., Chirichella, R., Cutini, A., and Chianucci, F. (2021). Characterizing the climatic niche of mast seeding in beech: evidences of trade-offs between vegetation growth and seed production. Ecol Indic 121, 107139.
Bergeron, P., Réale, D., Humphries, M.M., and Garant, D. (2011). Anticipation and tracking of pulsed resources drive population dynamics in eastern chipmunks. Ecol 92, 2027–2034.
Bogdziewicz, M., Zwolak, R., and Crone, E.E. (2016). How do vertebrates respond to mast seeding? Oikos 125, 300–307.
Bogdziewicz, M., Espelta, J.M., Muñoz, A., Aparicio, J.M., and Bonal, R. (2018a). Effectiveness of predator satiation in masting oaks is negatively affected by conspecific density. Oecologia 186, 983–993.
Bogdziewicz, M., Steele, M.A., Marino, S., and Crone, E.E. (2018b). Correlated seed failure as an environmental veto to synchronize reproduction of masting plants. New Phytol 219, 98–108.
Bogdziewicz, M., Marino, S., Bonal, R., Zwolak, R., and Steele, M.A. (2018c). Rapid aggregative and reproductive responses of weevils to masting of North American oaks counteract predator satiation. Ecol 99, 2575–2582.
Bogdziewicz, M., Ascoli, D., Hacket-Pain, A., Koenig, W.D., Pearse, I., Pesendorfer, M., Satake, A., Thomas, P., Vacchiano, G., Wohlgemuth, T., Tanentzap, A. (2020). From theory to experiments for testing the proximate mechanisms of mast seeding: an agenda for an experimental ecology. Ecol Lett 23: 210–220.
Boutin, S., Wauters, L.A., McAdam, A.G., Humphries, M.M., Tosi, G., and Dhondt, A. A. (2006). Anticipatory reproduction and population growth in seed predators. Science 314, 1928–1930.
Crawley, M.J., and Long, C.R. (1995). Alternate bearing, predator satiation and seedling recruitment in Quercus robur L. J Ecol 83, 683–696.
Dèath, G., and Fabricius, K.E. (2000). Classification and regression trees: a powerful yet simple technique for ecological data analysis. Ecol 81, 3178–3192.
Fletcher, Q.E., Boutin, S., Lane, J.E., LaMontagne, J.M., McAdam, A.G., Krebs, C.J., and Humphries, M.M. (2010). The functional response of a hoarding seed predator to mast seeding. Ecol 91, 2673–2683.
Gómez, J.M., Schupp, E.W., and Jordano, P. (2019). Synzoochory: the ecological and evolutionary relevance of a dual interaction. Biol Rev 94, 874–902.
Hanusch, M., He, X., Janssen, S., Selke, J., Trutschnig, W., and Junker, R.R. (2023). Exploring the frequency and distribution of ecological non-monotonicity in associations among ecosystem constituents. Ecosyst 26, 1819–1840.
Hou, X., Zhang, B., Chen, X., Wang J., Chen, Y., Chang, G. (2015). Influence of food abundance on distinguishing and dispersing of insect-infested Quercus glandulifera seeds by rodents (in Chinese). Sichuan J Zool 34: 846–851.
Hu, Y., Wang, X., Xu, Y., Yang, H., Tong, Z., Tian, R., Xu, S., Yu, L., Guo, Y., Shi, P., et al. (2023). Molecular mechanisms of adaptive evolution in wild animals and plants. Sci China Life Sci 66, 453–495.
Jansen, P.A., Forget, P.M. (2001). Scatter hoarding rodents and tree regeneration. In: Bongers, F., Charles-Dominique, P., Forget, P.M. and Théry, M. eds. Nouragues. Dordrecht: Springer, 275–288.
Kelly, D., and Sork, V.L. (2002). Mast seeding in perennial plants: why, how, where? Annu Rev Ecol Syst 33, 427–447.
Kelly, D., Koenig, W.D., and Liebhold, A.M. (2008). An intercontinental comparison of the dynamic behavior of mast seeding communities. Popul Ecol 50, 329–342.
Koenig, W.D., Mumme, R.L., Carmen, W.J., and Stanback, M.T. (1994). Acorn production by oaks in central coastal California: variation within and among years. Ecol 75, 99–109.
Li, H.J., and Zhang, Z.B. (2003). Effect of rodents on acorn dispersal and survival of the Liaodong oak (Quercus liaotungensis Koidz.). For Ecol Manage 176, 387–396.
Lian, J., Bai, Y., Qiu, Y., Bai, S., Guo, F. (2022). A review to the pests of Liaodong oak Quercus wutaishanica and the methods for pest control and prevention (in Chinese). Seed Sci Tech 40, 68–71.
Liang, K.Y., and Zeger, S.L. (1986). Longitudinal data analysis using generalized linear models. Biometrika 73, 13–22.
Lichti, N.I., Steele, M.A., Zhang, H., and Swihart, R.K. (2014). Mast species composition alters seed fate in North American rodent-dispersed hardwoods. Ecol 95, 1746–1758.
Lu, J., and Zhang, Z. (2004). Effects of habitat and season on removal and hoarding of seeds of wild apricot (Prunus armeniaca) by small rodents. Acta Oecol 26, 247–254.
Monks, A., Monks, J.M., and Tanentzap, A.J. (2016). Resource limitation underlying multiple masting models makes mast seeding sensitive to future climate change. New Phytol 210, 419–430.
Morales-Castilla, I., Matias, M.G., Gravel, D., and Araujo, M.B. (2015). Inferringbiotic interactions from proxies. Trends Ecol Evol 30, 347–356.
Moreira, X., Abdala-Roberts, L., Linhart, Y.B., and Mooney, K.A. (2014). Masting promotes individual- and population-level reproduction by increasing pollination efficiency. Ecol 95, 801–807.
Moreira, X., Pérez-Ramos, I.M., Abdala-Roberts, L., and Mooney, K.A. (2017). Functional responses of contrasting seed predator guilds to masting in two Mediterranean oak species. Oikos 126, 1042–1050.
Norton, D.A., and Kelly, D. (1988). Mast seeding over 33 years by Dacrydium cupressinum Lamb. (rimu) (Podocarpaceae) in New Zealand: the importance of economies of scale. Funct Ecol 2, 399–408.
Onodera, R., Akimoto, Y., Shimada, T., and Saitoh, T. (2017). Different population responses of three sympatric rodent species to acorn masting—the role of tannin tolerance. Popu Ecol 59, 29–43.
Ostfeld, R.S., and Keesing, F. (2000). Pulsed resources and community dynamics of consumers in terrestrial ecosystems. Trends Ecol Evol 15, 232–237.
Pearse, I.S., LaMontagne, J.M., Lordon, M., Hipp, A.L., and Koenig, W.D. (2020). Biogeography and phylogeny of masting: do global patterns fit functional hypotheses? New Phytol 227, 1557–1567.
Pélisson, P., Bernstein, C., François, D., Menu, F., and Venner, S. (2013). Dispersal and dormancy strategies among insect species competing for a pulsed resource. Ecol Entomol 38, 470–477.
Perea, R., López, D., San Miguel, A., and Gil, L. (2012). Incorporating insect infestation into rodent seed dispersal: better if the larva is still inside. Oecologia 170, 723–733.
Pesendorfer, M.B., Sillett, T.S., Koenig, W.D., and Morrison, S.A. (2016). Scatter-hoarding corvids as seed dispersers for oaks and pines: a review of a widely distributed mutualism and its utility to habitat restoration. Condor 118, 215–237.
Sachser, F., Pesendorfer, M., Gratzer, G., and Nopp-Mayr, U. (2021). Differential spatial responses of rodents to masting on forest sites with differing disturbance history. Ecol Evol 11, 11890–11902.
Sallabanks, R., and Courtney, S.P. (1992). Frugivory, seed predation, and insect-vertebrate interactions. Annu Rev Entomol 37, 377–400.
Soler, R., Espelta, J.M., Lencinas, M.V., Peri, P.L., and Martinez Pastur, G. (2017). Masting has different effects on seed predation by insects and birds in antarctic beech forests with no influence of forest management. For Ecol Manage 400, 173–180.
Steele, M.A. (2021). Oak seed dispersal: a study in plant-animal interactions. Baltimore: Johns Hopkins University Press.
Sun, S., Gao, X., and Chen, L. (2004). High acorn predation prevents the regeneration of Quercus liaotungensis in the Dongling mountain region of North China. Restor Ecol 12, 335–342.
Vander Wall, S.B. (2010). How plants manipulate the scatter-hoarding behaviour of seed-dispersing animals. Philos Trans R Soc Lond B Biol Sci 365, 989–997.
Visser, M.D., Muller-Landau, H.C., Wright, S.J., Rutten, G., and Jansen, P.A. (2011). Tri-trophic interactions affect density dependence of seed fate in a tropical forest palm. Ecol Lett 14, 1093–1100.
Wang, J., Zhang, B., Han, N., Feng, T., Hou, X., An, X., Chen, X., and Chang, G. (2021). Effects of mast seeding and insect infestation on predation and dispersal of Castanea mollissima nuts by rodents in the Qinling Mountains of China. For Ecol Manage 499, 119630.
Wang, W., Ma, K., and Liu, C. (1999). Removal and predation of Quercus liaotungensis acorns by animals. Ecol Res 14, 225–232.
Yan, C., and Zhang, Z. (2014). Specific non-monotonous interactions increase persistence of ecological networks. Proc R Soc B Biol Sci 281, 20132797.
Yan, C., and Zhang, Z. (2018a). Combined effects of intra- and inter-specific non-monotonic functions on the stability of a two-species system. Ecol Complex 33, 49–56.
Yan, C., and Zhang, Z. (2018b). Dome-shaped transition between positive and negative interactions maintains higher persistence and biomass in more complex ecological networks. Ecol Model 370, 14–21.
Yang, X., Zhang, H., and Zhang, Z. (2020a). Mast seeding and its relationship to animal hoarding behaviour. Biodivers Sci 28, 821–832.
Yang, X., Yan, C., Gu, H., and Zhang, Z. (2020b). Interspecific synchrony of seed rain shapes rodent-mediated indirect seed-seed interactions of sympatric tree species in a subtropical forest (in Chinese). Ecol Lett 23, 45–54.
Yang, Y., Wang, Z., Yan, C., Zhang, Y., Zhang, D., and Yi, X. (2018). Selective predation on acorn weevils by seed-caching Siberian chipmunk Tamias sibiricus in a tripartite interaction. Oecologia 188, 149–158.
Zeng, D., **, T., Zhao, Y., Yan, C., Zhang, Z., and Ding, P. (2021). Rodent abundance triggered switch between the relative mutualism and predation in a rodent-seed system of the subtropical island forest. Integr Zool 16, 109–119.
Zeng, D., Swihart, R.K., Zhao, Y., Si, X., Ding, P., Rees, M. (2019). Cascading effects of forested area and isolation on seed dispersal effectiveness of rodents on subtropical islands. J Ecol 107: 1506–1517.
Zhang, B., Chen, X., Steele, M.A., Li, J., and Chang, G. (2019). Effects of insect infestation on rodent-mediated dispersal of Quercus aliena: results from field and enclosure experiments. Integr Zool 14, 104–113.
Zhang, H., Chen, Y., and Zhang, Z. (2008). Differences of dispersal fitness of large and small acorns of Liaodong oak (Quercus liaotungensis) before and after seed caching by small rodents in a warm temperate forest, China. For Ecol Manage 255, 1243–1250.
Zhang, H., Yan, C., Chang, G., and Zhang, Z. (2016). Seed trait-mediated selection by rodents affects mutualistic interactions and seedling recruitment of co-occurring tree species. Oecologia 180, 475–484.
Zhang, H., Yan, C., Wu, S., Si, J., Yi, X., Li, H., and Zhang, Z. (2021b). Effects of masting on seedling establishment of a rodent-dispersed tree species in a warm-temperate region, northern China. Integr Zool 16, 97–108.
Zhang, H., Yan, C., Niu, H., Li, H., and Zhang, Z. (2022). Masting benefits seedling recruitment of Armeniaca sibirica through directed dispersal by rodents. For Ecol Manage 513, 120200.
Zhang, H., and Zhang, Z. (2008). Endocarp thickness affects seed removal speed by small rodents in a warm-temperate broad-leafed deciduous forest, China. Acta Oecol 34, 285–293.
Zhang, Z. (2003). Mutualism or cooperation among competitors promotes coexistence and competitive ability. Ecol Model 164, 271–282.
Zhang, Z., Yan, C., Krebs, C.J., and Stenseth, N.C. (2015). Ecological non-monotonicity and its effects on complexity and stability of populations, communities and ecosystems. Ecol Model 312, 374–384.
Zhang, Z., Yan, C., and Zhang, H. (2021a). Mutualism between antagonists: its ecological and evolutionary implications. Integr Zool 16, 84–96.
Zwolak, R., Bogdziewicz, M., Wrobel, A., and Crone, E.E. (2016). Advantages of masting in European beech: timing of granivore satiation and benefits of seed caching support the predator dispersal hypothesis. Oecologia 180, 749–758.
Zwolak, R., Celebias, P., and Bogdziewicz, M. (2022). Global patterns in the predator satiation effect of masting: a meta-analysis. Proc Natl Acad Sci USA 119, e2105655119.
Zwolak, R., Witczuk, J., Bogdziewicz, M., Rychlik, L., and Pagacz, S. (2018). Simultaneous population fluctuations of rodents in montane forests and alpine meadows suggest indirect effects of tree masting. J Mammal 99, 586–595.
Acknowledgement
This work was supported by the National Natural Science Foundation of China (32170508, 31772471), and the Fundamental Research Funds for the Central Universities (CCNU22LJ003). We thank F. Wang, Y. Luo, Z. Yang, Z. Wang, H. Gao, C. Yi, and X. Shang for their contributions to the field works.
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Zhang, H., Niu, H., Steele, M.A. et al. Masting promotes transformation from predation to mutualism in an oak-weevil-rodent system. Sci. China Life Sci. 67, 1514–1524 (2024). https://doi.org/10.1007/s11427-023-2517-1
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DOI: https://doi.org/10.1007/s11427-023-2517-1