The conservation physiology of seed dispersal

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 367, Issue 1596, 2012, Pages 1708-1718

  Ruxton, Graeme D ^a   Martin Schaefer, H ^b  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b UNIVERSITY OF FREIBURG   (Germany)

Author keywords

Digestive physiology; Environmental change; Mutualism; Rewilding; Seed dispersers

Indexed keywords

ANTHROPOGENIC EFFECT; CLIMATE CHANGE; CONSERVATION MANAGEMENT; ENVIRONMENTAL CHANGE; INVASIVE SPECIES; ISLAND; LAND USE CHANGE; MUTUALISM; POPULATION SIZE; RISK FACTOR; SEED DISPERSAL; SPECIALIZATION; TROPICAL ENVIRONMENT;

ANIMALIA;

EID: 84860701136     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2012.0001     Document Type: Review

References (74)

1. Clark, D. B., Clark, D. A. Read, J. M. 1998 Edaphic variation and the mesoscale distribution of tree species in a neotropical rain forest. J. Ecol. 86, 101-112 (doi:10.1046/j.1365-2745.1998.00238.x)
2. Howe, H. F. & Smallwood, J. 1982 Ecology of seed dispersal. Annu. Rev. Ecol. Syst. 13, 201-222 (doi:10.1146/annurev.es.13.110182.001221)
3. Janzen, D. H. 1970 Herbivores and number of treespecies in tropical forests. Am. Nat. 104,.501-528.(doi:10.1086/282687)
4. Connell, J. H. 1971 On the role of natural enemies in preventing exclusion in some marine animals and in rain forest trees. In Dynamics of populations (eds P. J. de Boer & G. R. Gradwell), pp. 298-312. Wageningen, The Netherlands: Centre for Agricultural Publishing and Documentation
5. Wenny, D. G. 2000 Seed dispersal, seed predation and seedling recruitment of a neotropical mountain tree. Ecol. Monogr. 70, 331-351 (doi:10.1890/0012-9615 (2000)070[0331:SDSPAS]2.0.CO;2)
6. Cousens, R., Wiegand, T. & Taghizadeh, M. 2008 Small-scale spatial structure within patterns of seed dispersal.Oceologia.158,.437-438.(doi:10.1007/s00442-008- 1150-7)
7. Jordano, P. & Schupp, E. W. 2000 Seed disperser effectiveness: the quantity component and patterns of seed rain for Prunus mahaleb. Ecol. Monogr. 70, 591-615.
8. Schaefer, H. M. & Ruxton, G. D. 2011 Plant animal communication. Oxford, UK: Oxford University Press
9. McAdoo, J. K., Evans, C. C., Roundy, B. A., Young, J. A. & Evans, R. A. 1983 Influence of heteromyid rodents on Oryzopsis hymenoides germination. J. Range Manag. 36, 61-64 (doi:10.2307/3897984)
10. Forget, P. M. 1992 Seed removal and seed fate in Gustavia superb.(Lecythidaceae). Biotropica.24, 408-414 (doi:10.2307/2388611)
11. Male, L. H. & Smulders, T. V. 2007 Hyperdispersed cache distributions reduce pilferage: a field study. Anim. Behav.73,.717-726.(doi:10.1016/j.anbehav.2006.06.017)
12. Vander Wall, S. B. 2010 How plants manipulate the scatter-hording behaviour of seed-dispersing animals. Phil. Trans. R. Soc. B 365, 989-997. (doi:10.1098/rstb. 2009.0205)
13. Levey, D. J. & Martinez Del Rio, C. 2001 It takes guts (and more) to eat fruit: lessons from avian nutritional ecology. Auk.118,.819-831.(doi:10.1642/0004- 8038(2001)118[0819:ITGAMT]2.0.CO;2)
14. Cazetta, E., Schaefer, H. M. & Galetti, M. 2008 Does attraction to frugivores or defense against pathogens shape fruit pulp composition? Oecologia 155, 277-286 (doi:10.1007/s00442-007-0917-6)
15. Whelan, C. J., Schmidt, K. A., Steele, B. B., Quinn, W. J. & Dilger, S. 1998 Are bird-consumed fruits complementary resources? Oikos 83, 195-205. (doi:10.2307/3546561)
16. Robertson, A. W., Trass, A., Ladley, J. J. & Kelly, D. 2006 Assessing the benefits of frugivory for seed germi- nation: the importance of the deinhibition effect. Funct. Ecol. 20, 58-66. (doi:10.1111/j.1365-2435.2005. 01057.x)
17. Samuels, I. A. & Levey, D. J. 2005 Effects of gut passage on seed germination: do experiments answer the questions they ask? Funct. Ecol. 19, 365-368. (doi:10.1111/ j.1365-2435.2005.00973.x)
18. Tewksbury, J. J., Levey, D. J., Huizinga, M., Haak, D. C. & Traveset, A. 2008.Costs and benefits of capsaicin-mediated control of gut retention in dispersers of wild chillies. Ecology 89, 107 -117. (doi:10.1890/07-0445.1)
19. Verdú, M. & Traveset, A. 2005 Early emergence enhances plant fitness: a phylogenetically controlled meta-analysis. Ecology 86, 1385-1394. (doi:10.1890/ 04-1647)
20. Rodríguez-Péres, J., Riera, N. & Traveset, A. 2005 Effect of seed passage through birds and lizards on emergence rate of Mediterranean species: differences between natu- ral and controlled conditions. Funct. Ecol. 19, 699-706. (doi:10.1111/j.0269-8463.2005.00971.x)
21. Wahaj, S. A., Levey, D. J., Sanders, A. K. & Cipollini, M. L. 1998 Control of gut retention time by secondary metabolites in ripe solanum fruits. Ecology.79, 2309- 2319.
22. Tewksbury, J. J., Huey, R. B. & Deutsch, C. A. 2008 Putting the heat on tropical animals. Science 320, 1296-1297. (doi:10.1126/science.1159328)
23. Traveset, A. 1999 The importance of mutualisms for bio-diversity conservation in insular ecosystems. Rev. Chilena Hist. Nat. 72, 527 - 538
24. Rick, C. M. & Bowman, R. I. 1961 Galapagos tomatoes and tortoises. Evolution 15,.407-417. (doi:10.2307/2406309)
25. Griffiths, C. J., Hansen, D. M., Jones, C. G., Zuel, N. & Harris, S. 2011 Resurrecting extant interactions with extant substitutes. Curr. Biol 21, 762-765. (doi:10.1016/j.cub.2011.03.042)
26. Popp, M., Mirré, V. & Brochmann, C. 2011 A single Mid-Pleiostocene long-distance dispersal by a bird can explain the extreme bipolar disjunction in crowberries (Empetrum). Proc. Natl Acad. Sci. USA 108, 6520-6525. (doi:10.1073/pnas.1012249108)
27. Jordano, P., Garcia, C., Godoy, J. A. & Garcia-Castano, J. L. 2007 Differential contribution of frugivores to complex seed dispersal patterns. Proc. Natl Acad. Sci. USA 104, 3278-3282. (doi:10.1073/pnas.0606793104)
28. Seidler, T. G. & Plotkin, J. B. 2006 Seed dispersal and spatial pattern in tropical plants. PLoS Biol. 4, 2132-2137. (doi:10.1371/journal.pbio.0040344)
29. Close, D. C. & McArthur, C. 2002 Rethinking the role of many plant phenolics: protection from photodamage not herbivores? Oikos 99, 166-172. (doi:10.1034/j.1600- 0706.2002.990117.x)
30. Schaefer, H. M., Schmidt, V. & Winkler, H. 2003 Testing the defence trade-off hypothesis: how contents of nutrients and secondary compounds affect fruit removal.Oikos 102, 318-328. (doi:10.1034/j.1600-0706.2003. 11796.x)
31. Mole, S., Ross, J. A. M. & Waterman, P. G. 1988 Light-induced variation in phenolic levels in foliage of rain-forest plants I. Chemical changes. J. Chem. Ecol. 14, 1-21. (doi:10.1007/BF01022527)
32. Cipollini, M. L., Paulk, E., Mink, K., Vaughn, K. & Fischer, T. 2004 Defense tradeoffs in fleshy fruits effects of resource variation on growth, reproduction and fruit secondary chemistry in Solanum carolinese. J. Chem. Ecol.30, 1-17. (doi:10.1023/B:JOEC.0000013179.45661.68)
33. Strauss, S. Y. & Whittall, J. B. 2006 Non-pollinator agents of selection on floral traits. In Ecology and evolution of flowers (eds L. D. Harder & S. C. H. Barrett), pp. 120-138. Oxford, UK: Oxford University Press.
34. Warren J. & Mackenzie, S. 2001 Why are all colour combinations not equally represented as flower colour olymorphisms? New Phytol. 151, 237-241. (doi:10. 1046/j.1469-8137.2001.00159.x)
35. Irwin, R. E., Strauss, S. Y., Storz, S., Emerson, A. & Guibert, G. 2003 The role of herbivores in the maintenance of a flower color polymorphism in wild radish. Ecology 84, 1733-1743. (doi:10.1890/0012-9658(2003) 084[1733:TROHIT]2.0.CO;2)
36. Bradshaw, H. D. & Schemske, W. 2003 Allele substitution at a flower colour locus produces a pollinator shift in monkeyflowers. Nature 426, 176-178. (doi:10. 1038/nature02106)
37. Montoya, D., Zavala, M. A., Rodriguez, M. A. & Purves, D. W. 2008 Animal versus wind dispersal and the robustness of tree species to deforestation. Science 320, 1502-1504. (doi:10.1126/science.1158404)
38. Alados, C. I., Navarro, T., Komac, B., Pascual, V. & Rietkerk, M. 2010 Dispersal abilities and spatial patterns in fragmented landscapes. Biol. J. Linn. Soc. 100, 935-947. (doi:10.1111/j.1095-8312.2010.01465.x)
39. Levey, D. J., Bolker, B. M., Tewksbury, J. J., Sargent, S. & Haddad, N. M. 2005 Effects of landscape corridors on seed dispersal by birds. Science 309, 146-148. (doi:10. 1126/science.1111479)
40. Restrepo, C., Gomez, N. & Heredia, S. 1999 Anthropogenic edges, treefall gaps, and fruit-frugivore interactions in a neotropical Montane forest. Ecology 80, 668-685
41. Damschen, E. I., Brudvig, L. A., Haddad, N. M., Levey, D. J., Orrock, J. L. & Tewksbury, J. J. 2008 The movement ecology and dynamics of plant communities in fragmented landscapes. Proc. Natl Acad. Sci. USA 105, 19078-19083. (doi:10.1073/pnas.0802037105)
42. Wotton, D. M. & Kelly, D. 2011 Frugivore loss limits recruitment of large-seeded trees. Proc. R. Soc. B 278, 3345-3354. (doi:10.1098/rspb.2011.0185)
43. Lefevre, K. L. & Rodd, F. H. 2009 How human disturbance of tropical rainforest can influence avian fruit removal? Oikos 118, 1405-1415 (doi:10.1111/j.1600- 0706.2009.17245.x)
44. Cordeiro, N. J. & Howe, H. F. 2001 Low recruitment of trees dispersed by animals in African forest fragments. Conserv. Biol. 15, 1733-1741. (doi:10.1046/j.1523- 1739.2001.99579.x)
45. Cordeiro, N. J. & Howe, H. F. 2003 Forest fragmentation severs mutualism between seed dispersers and an endemic African tree. Proc. Natl Acad. Sci. USA 100, 14052-14 056. (doi:10.1073/pnas.2331023100)
46. Zanini, L. & Ganade, G. 2005 Restoration of Araucaria forest: the role of perches, pioneer vegetation and soil fertility. Restor. Ecol. 13, 507-514. (doi:10.1111/j.1526- 100X.2005.00063.x)
47. Shiels, A. B. & Walker, L. R. 2003 Bird perches increase forest seeds on Puerto Rican landslides. Restor. Ecol. 11, 457-465. (doi:10.1046/j.1526-100X.2003.rec0269.x)
48. McConkey, K. M. & Drake, D. R. 2006 Flying foxes cease to function as seed dispersers long before they become rare. Ecology 87, 271 -276. (doi:10.1890/05-0386)
49. Fujita, M.S. & Tuttle, M. D. 1991 Flying foxes (Chiroptera, Pterodidae): threatened animals of key ecological and economic importance. Conserv. Biol. 5, 455-463. (doi:10.1111/j.1523-1739.1991.tb00352.x)
50. Wright, S. J., Stoner, K. E., Beckmann, N., Corlett, R. T.,Dirzo, R., Muller-Landau, H. C., Nunez-Iturri, G., Peres, C. A. & Wang, B. C. 2005 The plight of large ani- mals in tropical forests and the consequences for plant regeneration. Biotropica 39, 289-291. (doi:10.1111/j.1744-7429.2007.00293.x)
51. Redford, K. H. 1992 The empty forest. Bioscience 42, 412-422. (doi:10.2307/1311860)
52. Sekercioglu, C. H., Daily, G. C. & Ehrlich, P. R. 2004 Ecosystem consequences of bird declines. Proc. Natl. Acad. Sci. USA 101, 18042-18047. (doi:10.1073/ pnas.0408049101)
53. Ricciardi, A. & Simberloff, S. 2009 Assisted colonization is not a viable conservation strategy. Trends Ecol. Evol. 24, 248-253. (doi:10.1016/j.tree.2008.12.006)
54. Kaiser-Bunbury, C. N., Traveset, A. & Hansen, D. M. 2010 Conservation and restoration of plant-animal mutualisms on oceanic islands. Perspect. Plant Ecol. Evol. Syst. 12, 131-143. (doi:10.1016/j.ppees.2009.10.002)
55. Olesen, J. M. & Valido, A. 2003 Lizards as pollinators and seed dispersers: an island phenomenon. Trends Ecol. Evol. 18, 77-181. (doi:10.1016/S0169-5347(03)00004-1)
56. Kissling, W. D., Field, R., Korntheuer, H., Heyder, U. & Bohning-Gaese, K. 2010 Woody plants and the prediction of climate-change impacts on bird diversity. Phil. Trans. R. Soc. B 365, 2035-2045. (doi:10.1098/rstb. 2010.0008)
57. Anderson, J. T., Nuttle, T., Saldana Rojas, J. S., Pendergast, T. H. & Flecker, A. S. 2011 Extremely long-distance seed dispersal by an overfished Amazonian frugivore. Proc. R. Soc. B 278, 3309-3335. (doi:10. 1098/rspb.2011.0155)
58. Schaefer, H. M. & Schmidt, V. 2002 Feeding strategies and food intake of Blackcaps consuming ripe or unripe fruits and insects. J. Ornithol. 143, 341-350. (doi:10. 1046/j.1439-0361.2002.02018.x)
59. Menzel, A. 2003.Plant phenological anomalies in Germany and their relation to air temperature and NAO. Clim. Change.57,.243-263.(doi:10.1023/ A:1022880418362)
60. Pulido, F. & Widmer, M. 2005.Are long-distance migrants constrained in their evolutionary response to environmental change? Ann. NY Acad. Sci. 1046, 228-241. (doi:10.1196/annals.1343.020)
61. Corlett, R. T. 2007 The impact of hunting on the mammalian fauna of tropical Asian forests. Biotropica 39, 292-303. (doi:10.1111/j.1744-7429.2007.00271.x)
62. Hansen, D. M. & Muller, C. B. 2009 Invasive ants disrupt gecko pollination and seed dispersal of the endangered plant Roussea simplex in Mauritius. Biotropica 41, 202-308. (doi:10.1111/j.1744-7429.2008.00473.x)
63. Foster, J. T. & Robinson, S. K. 2007 Introduced birds and the fate of Hawaiian rainforests. Conserv. Biol. 21, 1248-1257. doi:10.1111/j.1523-1739.2007.00781.x
64. Hansen, D. M., Kaiser, C. N. & Muller, C. B. 2008 Seed dispersal and establishment of endangered plants on oceanic islands: he Janzen-Connell model and the use of ecological analogues. PLoS One 3, 1-9.
65. Riera, N., Traveset, A. & Garcia, O. 2004 Breakage of mutualisms by exotic species: the case of Cneorum tricoccon L. in the Balearic Islands (Western Mediterra- nean Sea). J. Biogeogr. 29, 713-719. (doi:10.1046/j.1365-2699.2002.00719.x)
66. Traveset, A. & Riera, N. 2004 Disruption of a plant-lizard seed dispersal system and its ecological effects on a threatened endemic plant in the Balearic Islands. Conserv. Biol. 19, 421-431. (doi:10.1111/j.1523-1739. 2005.00019.x)
67. Gosper, C. R., Stansbury, C. D. & Vivian-Smith, G. 2005 Seed dispersal of fleshy-fruited invasive plants by birds: contributing factors and management options. Divers. Distrib. 11, 549-558. (doi:10.1111/j.1366-9516. 2005.00195.x)
68. Cottam, Y. H., Merton, D. V. & Wouter, H. 2006 Nutrient composition of the diet of parent-raised kakapo nestlings. Notornis 53, 90-99.
69. Kissling, W. D., Rahbek, C. & Bohning-Gaese, K. 2007 Food plant diversity as a broad-scale determinant of avian frugivore richness. Proc. R. Soc. B 274, 799-808. (doi:10.1098/rspb.2006.0311)
70. Seebacher, F. & Franklin, C. E. 2012 Determining environmental causes of biological effects: the need for a mechanistic physiological dimension in conservation biology. Phil. Trans. R. Soc. B 367, 1607-1614. (doi:10.1098/rstb.2012.0036)
71. Moritz, C., Langham, G., Kearney, M., Krockenberger, A., VanDerWal, J. & Williams, S. 2012 Integrating phylogeography and physiology reveals divergence of thermal traits between central and peripheral lineages of tropical rainforest lizards. Phil. Trans. R. Soc. B 367, 1680-1687. (doi:10.1098/rstb.2012.0018)
72. Klaassen, M., Hoye, B. J., Nolet, B. A. & Buttemer, W. A. 2012 Ecophysiology of avian migration in the face of current global hazards. Phil. Trans. R. Soc. B 367, 1719-1732. (doi:10.1098/rstb.2012.0008)
73. Blaustein, A. R., Gervasi, S. S., Johnson, P. T. J., Hoverman, J. T., Belden, L. K., Bradley, P. W. & Xie, G. Y. 2012 Ecophysiology meets conservation: under- standing the role of disease in amphibian population declines. Phil. Trans. R. Soc. B 367, 1688-1707. (doi:10.1098/rstb.2012.0011)
74. Brauner, C. J., Sackville, M., Gallagher, Z., Tang, S., Nendick, L. & Farrell, A. P. 2012 Physiological consequences of the salmon louse (Lepeophtheirus salmonis) on juvenile pink salmon (Oncorhynchus gorbuscha): impli- cations for wild salmon ecology and management, and for salmon culture. Phil. Trans. R. Soc. B 367, 1770-1779. (doi:10.1098/rstb.2011.0423)