Masting behaviour in a Mediterranean pine tree alters seed predator selection on reproductive output

Plant Biology

Volumn 18, Issue 6, 2016, Pages 973-980

  Moreira, X ^a   Abdala Roberts, L ^b   Zas, R ^a   Merlo, E ^c   Lombardero, M J ^d   Sampedro, L ^a   Mooney, K A ^e  

^a MISIÓN BIOLÓGICA DE GALICIA CSIC   (Spain)

^b Univ Aut noma de Yucatán   (Mexico)

^c Madera Plus Company   (Spain)

^d UNIVERSITY OF SANTIAGO DE COMPOSTELA   (Spain)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Density dependence; functional response; genotype; Pinus pinaster; predator satiation hypothesis; seed cones

Indexed keywords

CONIFEROUS TREE; DENSITY DEPENDENCE; FUNCTIONAL RESPONSE; GENOTYPE; MASTING; MEDITERRANEAN ENVIRONMENT; REPRODUCTIVE PRODUCTIVITY; SEED PREDATION;

ANIMALIA; PINUS PINASTER;

ANIMAL; BIOMASS; EVOLUTION; FEEDING BEHAVIOR; FOREST; GENOTYPE; GROWTH, DEVELOPMENT AND AGING; PHYSIOLOGY; PINE; PLANT SEED; PREDATION; REPRODUCTION; SATIETY;

ANIMALS; BIOLOGICAL EVOLUTION; BIOMASS; FEEDING BEHAVIOR; FORESTS; GENOTYPE; PINUS; PREDATORY BEHAVIOR; REPRODUCTION; SATIATION; SEEDS;

EID: 84991658422     PISSN: 14358603     EISSN: 14388677     Source Type: Journal    
DOI: 10.1111/plb.12491     Document Type: Article

References (55)

1. Abdala-Roberts L., Mooney K.A. (2014) Ecological and evolutionary consequences of plant genotype diversity in a tri-trophic system. Ecology, 95, 2879–2893.
2. Abdala-Roberts L., Mooney K.A. (2015) Plant and herbivore evolution within the trophic sandwich. In: Hanley T. C. N., La Pierre K. J. (Eds), Trophic interactions: bottom-up and top-down interactions in aquatic and terrestrial ecosystems. Cambridge University Press, Cambridge, UK, pp 339–363.
3. Abdala-Roberts L., Parra-Tabla V., Campbell D.R., Mooney K.A. (2014) Soil fertility and parasitoids shape herbivore selection on plants. Journal of Ecology, 102, 1120–1128.
4. Abrahamson W.G. (1989) Plant–animal interactions. McGraw-Hill, New York, NY, USA.
5. Abrams P.A. (1982) Functional responses of optimal foragers. The American Naturalist, 120, 382–390.
6. Abrams P.A. (2000) The evolution of predator–prey interactions: theory and evidence. Annual Review of Ecology, Evolution and Systematics, 31, 79–105.
7. Agrawal A.A. (2005) Natural selection on common milkweed (Asclepias syriaca) by a community of specialized insect herbivores. Evolutionary Ecology Research, 7, 651–667.
8. Archibald D.W., McAdam A.G., Boutin S., Fletcher Q.E., Humphries M.M. (2012) Within-season synchrony of a masting conifer enhances seed escape. The American Naturalist, 179, 536–544.
9. Bogdziewicz M., Zwolak R., Crone E.E. (2016) How do vertebrates respond to mast seeding? Oikos, 125, 300–307.
10. Chesson P., Gebauer R.L.E., Schwinning S., Huntly N., Wiegand K., Ernest M.S.K., Sher A., Novoplansky A., Weltzin J.F. (2004) Resource pulses, species interactions, and diversity maintenance in arid and semi-arid environments. Oecologia, 141, 236–253.
11. Espelta J.M., Bonal R., Sánchez-Humanes B. (2009) Pre-dispersal acorn predation in mixed oak forests: Interspecific differences are driven by the interplay among seed phenology, seed size and predator size. Journal of Ecology, 97, 1416–1423.
12. Fletcher Q.E., Boutin S., Lane J.E., LaMontagne J.M., McAdam A.G., Krebs C.J., Humphries M.M. (2010) The functional response of a hoarding seed predator to mast seeding. Ecology, 91, 2673–2683.
13. Friman V.-P., Laakso J. (2011) Resource dynamics constrain the evolution of predator–prey interactions. The American Naturalist, 177, 334–345.
14. Gómez J.M. (2003) Herbivory reduces the strength of pollinator-mediated selection in the Mediterranean herb Erysimum mediohispanicum: consequences for plant specialization. The American Naturalist, 162, 242–256.
15. Herrera C.M., Medrano M., Rey P.J., Sanchez-Lafuente A.M., Garcia M.B., Guitian J., Manzaneda A.J. (2002) Interaction of pollinators and herbivores on plant fitness suggests a pathway for correlated evolution of mutualism- and antagonism-related traits. Proceedings of the National Academy of Sciences USA, 99, 16823–16828.
16. Holling C.S. (1959) The components of predation as revealed by a study of small mammal predation of the European pine sawfly. Canadian Entomologist, 91, 293–320.
17. Holling C.S. (1965) The functional response of predators to prey density and its role in mimicry and population regulation. Memoirs of the Entomological Society of Canada, 48, 3–86.
18. terHorst C.P., Lau J.A., Cooper I.A., Keller K.R., La Rosa R.J., Royer A.M., Schultheis E.H., Suwa T., Conner J.K. (2015) Quantifying non-additive selection caused by indirect ecological effects. Ecology, 96, 2360–2369.
19. Janzen D.H. (1976) Why bamboos wait so long to flower. Annual Review of Ecology and Systematics, 7, 347–391.
20. Johnson M.T.J., Stinchcombe J.R. (2007) An emerging synthesis between community ecology and evolutionary biology. Trends in Ecology & Evolution, 22, 250–257.
21. Jones F.A., Comita L.S. (2010) Density-dependent pre-dispersal seed predation and fruit set in a tropical tree. Oikos, 119, 1841–1847.
22. Juliano S.A. (2001) Non-linear curve fitting: predation and functional response curves. In: Scheiner S. M., Gurevitch J. (Eds), Design and analysis of ecological experiments. Oxford University Press, New York, USA, pp 178–196.
23. Kelly D. (1994) The evolutionary ecology of mast seeding. Trends in Ecology & Evolution, 9, 465–470.
24. Kolb A., Ehrlén J. (2010) Environmental context drives seed predator-mediated selection on a floral display trait. Evolutionary Ecology, 24, 433–445.
25. LaMontagne J.M., Boutin S. (2009) Quantitative methods for defining mast-seeding years across species and studies. Journal of Vegetation Science, 20, 745–753.
26. Lande R., Arnold R. (1983) The measurement of selection on correlated characters. Evolution, 37, 1210–1226.
27. Leimu R., Syrjänen K., Ehrlén J., Lehtilä K. (2002) Pre-dispersal seed predation in Primula veris: among-population variation in damage intensity and selection on flower number. Oecologia, 133, 510–516.
28. Linhart Y.B., Moreira X., Snyder M.A., Mooney K.A. (2014) Variability in seed cone production and functional response of seed predators to seed cone availability: support for the predator satiation hypothesis. Journal of Ecology, 102, 576–583.
29. Littell R.C., Milliken G.A., Stroup W.W., Wolfinger R., Schabenberger O. (2006) SAS System for mixed models2nd edn. SAS, Cary, NC, USA.
30. Maron J.L., Baer K.C., Angert A.L. (2014) Disentangling the drivers of context-dependent plant–animal interactions. Journal of Ecology, 102, 1485–1496.
31. Mezquida E.T., Rodríguez-García E., Olano J.M. (2016) Efficiency of pollination and satiation of predators determine reproductive output in Iberian Juniperus thurifera woodlands. Plant Biology, 18, 147–155.
32. Miller T.E.X., Tenhumberg B., Louda S.M. (2008) Herbivore-mediated ecological costs of reproduction shape the life history of an iteroparous plant. The American Naturalist, 171, 141–149.
33. Moreira X., Abdala-Roberts L., Linhart Y.B., Mooney K.A. (2014) Masting promotes individual- and population-level reproduction by increasing pollination efficiency. Ecology, 95, 801–807.
34. Moreira X., Abdala-Roberts L., Linhart Y.B., Mooney K.A. (2015) Effects of climate on reproductive investment in a masting species: assessment of climatic predictors and underlying mechanisms. Journal of Ecology, 103, 1317–1324.
35. Ostfeld R.S., Keesing F. (2000) Pulsed resources and community dynamics of consumers in terrestrial ecosystems. Trends in Ecology & Evolution, 15, 232–237.
36. Pearse I.S., Koenig W.D., Knops J.M.H. (2014) Cues versus proximate drivers: testing the mechanism behind masting behavior. Oikos, 123, 179–184.
37. Pesendorfer M.B., Koenig W.D. (2016) The effect of within-year variation in acorn crop size on seed predation and dispersal by avian hoarders. Oecologia, 181, 97–106.
38. Polis G.A., Power M.E., Huxel G.R. (2004) Food webs at the landscape level. University of Chicago Press, Chicago, IL, USA.
39. Price P.W., Lewinsohn T.M., Fernandes W., Benson W.W. (1991) Plant–animal interactions: evolutionary ecology in tropical and temperate regions. John Wiley and Sons, New York, NY, USA.
40. Rausher M.D. (1992) The measurement of selection on quantitative traits: biases due to environmental covariances between traits and fitness. Evolution, 46, 616–626.
41. Rausher M.D., Simms E.L. (1989) The evolution of resistance to herbivory in Ipomoea purpurea. I. Attempts to detect selection. Evolution, 43, 563–572.
42. Richardson D.M. (1998) Ecology and biogeography of Pinus. Cambridge University Press, Cambridge, UK, pp.556.
43. Salgado-Luarte C., Gianoli E. (2012) Herbivores modify selection on plant functional traits in a temperate rainforest understory. The American Naturalist, 180, E42–E53.
44. Siepielski A.M., Benkman C.W. (2008) Seed predation and selection exerted by a seed predator influence subalpine tree densities. Ecology, 89, 2960–2966.
45. Silvertown J.W. (1980) The evolutionary ecology of mast-seeding in trees. Biological Journal of the Linnean Society, 14, 235–250.
46. Sletvold N., Moritz K.K., Ågren J. (2015) Additive effects of pollinators and herbivores result in both conflicting and reinforcing selection on floral traits. Ecology, 96, 214–221.
47. Stinchcombe J.R. (2005) Measuring natural selection on proportional traits: comparisons of three types of selection estimates for resistance and susceptibility to herbivore damage. Evolutionary Ecology, 19, 363–373.
48. Stinchcombe J.R., Rausher M.D. (2002) The evolution of tolerance to deer herbivory: modifications caused by the abundance of insect herbivores. Proceedings of the Royal Society, Series B, 269, 1241–1246.
49. Stinchcombe J.R., Rutter M.T., Burdick D.S., Tiffin P., Rausher M.D., Mauricio R. (2002) Testing for environmentally induced bias in phenotypic estimates of natural selection: theory and practice. The American Naturalist, 160, 511–523.
50. Strauss S.Y., Irwin R.E. (2004) Ecological evolutionary consequences of multi-species interactions. Annual Review of Ecology, Evolution, & Systematics, 35, 435–466.
51. Thompson J.N. (1999) The evolution of species interactions. Science, 284, 2116–2118.
52. Trexler J.C., McCulloch C.E., Travis J. (1988) How can the functional response best be determined? Oecologia, 76, 206–214.
53. Valverde P.L., Fornoni J., Núñez-Farfán J. (2001) Defensive role of leaf trichomes in resistance to herbivorous insects in Datura stramonium. Journal of Evolutionary Biology, 14, 424–432.
54. Yang L.H., Bastow J.L., Spence K.O., Wright A.N. (2008) What can we learn from resource pulses? Ecology, 89, 621–634.
55. Zwolak R., Bogdziewicz M., Wróbel A., 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.