Advantages of masting in European beech: timing of granivore satiation and benefits of seed caching support the predator dispersal hypothesis

Oecologia

Volumn 180, Issue 3, 2016, Pages 749-758

  Zwolak, Rafał ^a   Bogdziewicz, Michał ^a   Wróbel, Aleksandra ^a   Crone, Elizabeth E ^b,c  

^a ADAM MICKIEWICZ UNIVERSITY   (Poland)

^b HARVARD UNIVERSITY   (United States)

^c TUFTS UNIVERSITY   (United States)

Author keywords

Apodemus flavicollis; Fagus sylvatica; Granivory; Scatterhoarding; Seed dispersal

Indexed keywords

CACHING; DECIDUOUS TREE; FOREST FLOOR; GRANIVORY; MASTING; PLANT-HERBIVORE INTERACTION; POLLINATION; RODENT; SEED DISPERSAL; SEEDLING EMERGENCE;

APODEMUS FLAVICOLLIS; FAGUS; FAGUS SYLVATICA; MUS; RODENTIA; VERTEBRATA;

ANIMAL; BEECH; EUROPE; EVOLUTION; FEEDING BEHAVIOR; GROWTH, DEVELOPMENT AND AGING; MOUSE; MURINE; PHYSIOLOGY; PLANT SEED; PREDATION; REPRODUCTION; SATIETY; SEED DISPERSAL;

ANIMALS; BIOLOGICAL EVOLUTION; EUROPE; FAGUS; FEEDING BEHAVIOR; MICE; MURINAE; PREDATORY BEHAVIOR; REPRODUCTION; SATIATION; SEED DISPERSAL; SEEDS;

EID: 84959487319     PISSN: 00298549     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00442-015-3511-3     Document Type: Article

References (67)

1. Allen RB, Mason NW, Richardson SJ, Platt KH (2012) Synchronicity, periodicity and bimodality in inter-annual tree seed production along an elevation gradient. Oikos 121:367–376
2. Barringer LE, Tomback DF, Wunder MB, McKinney ST (2012) Whitebark pine stand condition, tree abundance, and cone production as predictors of visitation by Clark’s nutcracker. PLoS One 7:e37663
3. Bates D, Maechler M, Bolker B, Walker S (2013) lme4: linear mixed-effects models using Eigen and S4. R package version 1.0-4. http://CRAN.R-project.org/package=lme4
4. Briggs JS, Vander Wall SB, Jenkins SH (2009) Forest rodents provide directed dispersal of Jeffrey pine seeds. Ecology 90:675–687
5. Crawley M, Long C (1995) Alternate bearing, predator satiation and seedling recruitment in Quercus robur L. J Ecol 83:683–696
6. Crone EE, McIntire MJB, Brodie J (2011) What defines mast seeding? Spatio-temporal patterns of cone production by whitebark pine. J Ecol 99:438–444
7. Curran LM, Leighton M (2000) Vertebrate responses to spatiotemporal variation in seed production of mast-fruiting dipterocarpaceae. Ecol Monogr 70:101–128
8. Dróżdż A (1966) Food habits and food supply of rodents in the beech forest. Acta Theriol 16:363–384
9. Espelta JM, Cortés P, Molowny-Horas R, Sánchez-Humanes B, Retana J (2008) Masting mediated by summer drought reduces acorn predation in Mediterranean oak forests. Ecology 89:805–817
10. Fletcher QE, Boutin S, Lane JE, LaMontagne JM, McAdam AG, Krebs CJ, Humphries MM (2010) The functional response of a hoarding seed predator to mast seeding. Ecology 91:2673–2683
11. Grodziński W, Sawicka-Kapusta K (1970) Energy values of tree-seeds eaten by small mammals. Oikos 21:52–58
12. Herrera CM, Jordano P, Guitián J, Traveset A (1998) Annual variability in seed production by woody plants and the masting concept: reassessment of principles and relationship to pollination and seed dispersal. Am Nat 152:576–594
13. Hilton G, Packham J (1997) A sixteen-year record of regional and temporal variation in the fruiting of beech (Fagus sylvatica L.) in England (1980–1995). Forestry 70:7–16
14. Hirsch BT, Kays R, Jansen PA (2012) A telemetric thread tag for tracking seed dispersal by scatter-hoarding rodents. Plant Ecol 213:933–943
15. Hoshizaki K, Hulme PE, Levey DJ, Silwa WR, Galetti M (2002) Mast seeding and predator-mediated indirect interactions in a forest community: evidence from post-dispersal fate of rodent-generated caches. In: Levey D, Silva W, Galetti M (eds) Seed dispersal and frugivory: ecology, evolution and conservation. CABI, Wallingford, pp 227–239
16. Hulme PE, Kollmann J (2005) Seed predator guilds, spatial variation in post-dispersal seed predation and potential effects on plant demography: a temperate perspective. In: Forget PM, Lambert JE, Hulme PE, Vander Wall SB (eds) Seed fate: predation and secondary dispersal. CABI, Wallingford, pp 9–30
17. Jansen PA, Forget P-M (2001) Scatterhoarding rodents and tree regeneration. In: Bongers F, Charles-Dominique P, Forget PM, Théry M (eds) Nouragues: dynamics and plant–animal interactions in a neotropical rainforest. Springer, Berlin, pp 275–288
18. Jansen PA, Bongers F, Hemerik L (2004) Seed mass and mast seeding enhance dispersal by a neotropical scatter-hoarding rodent. Ecol Monogr 74:569–589
19. Jansen PA, Bongers F, van der Meer J (2008) Is farther seed dispersal better? Spatial patterns of offspring mortality in three rainforest tree species with different dispersal abilities. Ecography 31:43–52
20. Janzen DH (1971) Seed predation by animals. Annu Rev Ecol Syst 2:465–492
21. Jensen TS (1982) Seed production and outbreaks of non-cyclic rodent populations in deciduous forests. Oecologia 54:184–192
22. Jensen TS (1985) Seed-seed predator interactions of European beech, Fagus silvatica and forest rodents, Clethrionomys glareolus and Apodemus flavicollis. Oikos 44:149–156
23. Kelly D (1994) The evolutionary ecology of mast seeding. Trends Ecol Evol 9:465–470
24. Kelly D, Sork VL (2002) Mast seeding in perennial plants: why, how, where? Annu Rev Ecol Syst 33:427–447
25. Kelly D, Hart DE, Allen RB (2001) Evaluating the wind pollination benefits of mast seeding. Ecology 82:117–126
26. Koenig WD, Knops JM (2013) Large-scale spatial synchrony and cross-synchrony in acorn production by two California oaks. Ecology 94:83–93
27. Koenig WD, Mumme RL, Carmen WJ, Stanback MT (1994) Acorn production by oaks in central coastal California: variation within and among years. Ecology 75:99–109
28. Li H, Zhang Z (2003) Effect of rodents on acorn dispersal and survival of the Liaodong oak (Quercus liaotungensis Koidz.). For Ecol Manag 176:387–396
29. Li H, Zhang Z (2007) Effects of mast seeding and rodent abundance on seed predation and dispersal by rodents in Prunus armeniaca (Rosaceae). For Ecol Manage 242:511–517
30. Ligon JD (1978) Reproductive interdependence of piñon jays and piñon pines. Ecol Monogr 48:111–126
31. Linhart YB, Moreira X, Snyder MA, Mooney KA (2014) Variability in seed cone production and functional response of seed predators to seed cone availability: support for the predator satiation hypothesis. J Ecol 102:576–583
32. Liu X, Etienne RS, Liang M, Wang Y, Yu S (2015) Experimental evidence for an intraspecific Janzen–Connell effect mediated by soil biota. Ecology 96:662–671
33. Maeto K, Ozaki K (2003) Prolonged diapause of specialist seed-feeders makes predator satiation unstable in masting of Quercus crispula. Oecologia 137:392–398
34. McKinney ST, Tomback DF (2007) The influence of white pine blister rust on seed dispersal in whitebark pine. Can J For Res 37:1044–1057
35. Moore JE, Swihart RK (2007) Importance of fragmentation-tolerant species as seed dispersers in disturbed landscapes. Oecologia 151:663–674
36. Moore JE, McEuen AB, Swihart RK, Contreras TA, Steele MA (2007) Determinants of seed removal distance by scatter-hoarding rodents in deciduous forests. Ecology 88:2529–2540
37. Moreira X, Abdala-Roberts L, Linhart YB, Mooney KA (2014) Masting promotes individual- and population-level reproduction by increasing pollination efficiency. Ecology 95:801–807
38. Moreira X, Abdala-Roberts L, Linhart YB, Mooney KA (2015) Effects of climate on reproductive investment in a masting species: assessment of climatic predictors and underlying mechanisms. J Ecol 103:1317–1324
39. Nilsson SG (1985) Ecological and evolutionary interactions between reproduction of beech Fagus sylvatica and seed eating animals. Oikos 44:157–164
40. Nilsson SG, Wästljung U (1987) Seed predation and cross-pollination in mast-seeding beech (Fagus sylvatica) patches. Ecology 68:260–265
41. Packham JR, Thomas PA, Atkinson MD, Degen T (2012) Biological flora of the British Isles: Fagus sylvatica. J Ecol 100:1557–1608
42. Pearse IS, Koenig WD, Knops JMH (2014) Cues versus proximate drivers: testing the mechanism behind masting behavior. Oikos 123:179–184
43. Pidek IA, Svitavská-Svobodová H, van der Knaap WO, Noryśkiewicz AM, Filbrandt-Czaja A et al (2010) Variation in annual pollen accumulation rates of Fagus along a N-S transect in Europe based on pollen traps. Veg Hist Archaeobot 19:259–270
44. Puerta-Piñero C, Gómez JM, Schupp EW (2010) Spatial patterns of acorn dispersal by rodents: do acorn crop size and ungulate presence matter? Oikos 119:179–187
45. Rapp JM, McIntire EJB, Crone EE (2013) Sex allocation, pollen limitation and masting in whitebark pine. J Ecol 101:1345–1352
46. Silvertown JW (1980) The evolutionary ecology of mast seeding in trees. Biol J Linn Soc 14:235–250
47. Sork VT (1984) Examination of seed dispersal and survival in red oak, Quercus rubra (Fagaceae), using metal-tagged acorns. Ecology 65:1020–1022
48. Standovár T, Kenderes K (2003) A review on natural stand dynamics in beechwoods of east central Europe. Appl Ecol Environ Res 1:19–46
49. Stapanian MA, Smith CC (1978) A model for seed scatterhoarding: coevolution of fox squirrels and black walnuts. Ecology 59:884–896
50. Swamy V, Terborgh J, Dexter KG, Best BD, Alvarez P, Cornejo F (2011) Are all seeds equal? Spatially explicit comparisons of seed fall and sapling recruitment in a tropical forest. Ecol Lett 14:195–201
51. Tachiki Y, Iwasa Y (2010) Both seedling banks and specialist seed predators promote the evolution of synchronized and intermittent reproduction (masting) in trees. J Ecol 98:1398–1408
52. Theimer TC (2001) Seed scatterhoarding by white-tailed rats: consequences for seedling recruitment by an Australian rain forest tree. J Trop Ecol 17:177–189
53. Theimer TC (2005) Rodent scatterhoarders as conditional mutualists. In: Forget PM, Lambert JE, Hulme PE, Vander Wall SB (eds) Seed fate: predation and secondary dispersal. CABI, Wallingford, pp 283–295
54. Turnbull MH, Pharis RP, Kurepin LV, Sarfati M, Mander LN, Kelly D (2012) Flowering in snow tussock (Chionochloa spp.) is influenced by temperature and hormonal cues. Funct Plant Biol 39:38–50
55. Vander Wall SB (1994) Seed fate pathways of antelope bitterbrush: dispersal by seed-caching yellow pine chipmunks. Ecology 75:1911–1926
56. Vander Wall SB (2001) The evolutionary ecology of nut dispersal. Bot Rev 67:74–117
57. Vander Wall SB (2002) Masting in animal-dispersed pines facilitates seed dispersal. Ecology 83:3508–3516
58. Vander Wall SB (2010) How plants manipulate the scatter-hoarding behaviour of seed-dispersing animals. Philos Trans R Soc B 365:989–997
59. Vander Wall SB, Balda RP (1977) Coadaptations of the Clark’s nutcracker and the pinon pine for efficient seed harvest and dispersal. Ecol Monogr 47:89–111
60. Visser MD, Jongejans E, van Breugel M, Zuidema PA, Chen YY, Kassim AR, de Kroon H (2011) Strict mast fruiting for a tropical dipterocarp tree: a demographic cost–benefit analysis of delayed reproduction and seed predation. J Ecol 99:1033–1044
61. Wróbel A, Zwolak R (2013) The choice of seed tracking method influenced fate of beech seeds dispersed by rodents. Plant Ecol 214:471–475
62. Xiao Z, Jansen PA, Zhang Z (2006) Using seed-tagging methods for assessing post-dispersal seed fate in rodent-dispersed trees. For Ecol Manage 223:18–23
63. Xiao Z, Zhang Z, Krebs CJ (2013) Long-term seed survival and dispersal dynamics in a rodent-dispersed tree: testing the predator satiation hypothesis and the predator dispersal hypothesis. J Ecol 101:1256–1264
64. Yi X, Yang YQ, Zhang ZB (2011) Intra-and inter-specific effects of mast seeding on seed fates of two sympatric Corylus species. Plant Ecol 212:785–793
65. Zwolak R, Crone EE (2012) Quantifying the outcome of plant–granivore interactions. Oikos 121:20–27
66. Zwolak R, Bogdziewicz M, Rychlik L (2016) Beech masting modifies the response of rodents to forest management. For Ecol Manag 359:268–276
67. Żywiec M, Holeksa J, Ledwoń M, Seget P (2013) Reproductive success of individuals with different fruit production patterns. What does it mean for the predator satiation hypothesis? Oecologia 172:461–467