Is the inverse leafing phenology of the dry forest understory shrub Jacquinia nervosa (Theophrastaceae) a strategy to escape herbivory?

Revista de Biologia Tropical

Volumn 54, Issue 3, 2006, Pages 951-963

  Chaves, Óscar M ^a   Avalos, Gerardo ^a,b  

^a UNIVERSIDAD DE COSTA RICA   (Costa Rica)

^b Center for Sustainable Development Studies   (United States)

Author keywords

Escape hypothesis; Insect herbivory; Inverse phenology; Jacquinia nervosa; Tropical dry forest

Indexed keywords

BONELLIA NERVOSA; CHRYSOMELIDAE; COLEOPTERA; COPTOCYCLA RUFONOTATA; EPICAUTA; HEXAPODA; LEPIDOPTERA; MELOIDAE; PHYLLANTHUS (ANGIOSPERM); THEOPHRASTACEAE; TORTRICIDAE;

ADAPTATION; ANGIOSPERM; ANIMAL; ARTICLE; BEETLE; COSTA RICA; GERMINATION; GROWTH, DEVELOPMENT AND AGING; PHOTOPERIODICITY; PHYSIOLOGY; PREDATION; SEASON; TREE;

ADAPTATION, PHYSIOLOGICAL; ANGIOSPERMS; ANIMALS; BEETLES; COSTA RICA; GERMINATION; PHOTOPERIOD; PREDATORY BEHAVIOR; SEASONS; TREES;

EID: 52149122109     PISSN: 00347744     EISSN: 22152075     Source Type: Journal    
DOI: 10.15517/rbt.v54i3.14074     Document Type: Article

References (90)

1. Aide, T. M. 1988. Herbivory as a selective agent on the timing of leaf production in a tropical understory community. Nature 336: 574-575.
2. Aide, T. M. 1992. Dry season leaf production: an escape from herbivory. Biotropica 24: 532-537.
3. Augspurger, C. K. 1981. Reproductive synchrony of a tropical shrub: experimental studies on effects of pollinators and seed predators on Hybanthus prunifolius (Violaceae). Ecology 62: 775-778.
4. Augspurger, C. K. 1983. Phenology, flowering synchrony, and fruit set of six neotropical shrubs. Biotropica 15: 257-267.
5. Augspurger, C. K. 1990. Una señal para la floración sincrónica, p. 201-218. In E. G. Leigh Jr., A. S. Rand & D. M. Windsor (eds.). Ecología de un Bosque Tropical: ciclos estacionales y cambios a largo plazo. Instituto Smithsonian de Investigaciones Tropicales, Panamá, Panamá.
6. Barone, J. A. & P. D. Coley. 2002. Herbivorismo y las defensas de las plantas, p. 464-492. In M. R. Guariguata & G. H. Kattan (eds.). Ecología y conservación de bosques neotropicales. LUR, San José, Costa Rica.
7. Bawa, K. S. 1974. Breeding systems of tree species of a lowland tropical community. Evolution 28: 85-92.
8. Bazzaz, F. A., N. R. Chiariello, P. D. Coley & L. F. Pitelka. 1987. Allocating resources to reproduction and defense. Bioscience 37: 58-66.
9. Bloem, K. A., K. C. Kelley & S. S. Duffey. 1989. Differential effect of tomatine and its alleviation by cholesterol on larval growth and efficiency of food utilization in Heliothis zea and Spodoptera exigua. J. Chem. Ecol. 15: 387-398.
10. Borchert, R. 1983. Phenology and control of flowering in tropical trees. Biotropica 15: 81-89.
11. Borchert, R. 1994. Soil and stem water storage determine phenology and distribution of tropical dry forest trees. Ecology 75: 1437-1449.
12. Borchert, R. 1995. Phenology and flowering periodicity of neotropical dry forest species: evidence from herbarium collections.
13. Borchert, R. 1999. Climatic periodicity, phenology, and cambium activity in tropical dry forest trees. IAWA J. 20: 239-247.
14. Borchert, R., G. Rivera & W. Hagnauer. 2002. Modification of vegetative phenology in a Tropical Semi-deciduous Forest by abnormal drought and rain. Biotropica 34: 27-39.
15. Borchert, R., S. S. Renner, Z. Calle, D. Navarrete, A. Tye, L. Gautier, R. Spichiger & P. von Hildebrand. 2005. Photoperiodic induction of synchronous flowering near the Equator. Nature 433: 627-629.
16. Braker, E. & R. L. Chazdon. 1993. Ecological, behavioural, and nutritional factors influencing use of palms as host plants by a Neotropical forest grasshopper. J. Trop. Ecol. 9: 181-195.
17. Brodribb, T. J. & N. M. Holbrook. 2003. Stomatal closure during leaf dehydration, correlation with other leaf physiological traits. Plant Physiol. 132: 2166-2173.
18. Brown, V. K., A. C. Gange, I. M. Evans & A. L. Storr. 1987. The effect of insect herbivory on the grown and reproduction of two annual Vicia species at different stages in plant succession. J. Ecol. 75: 1173-1189.
19. Coley, P. D. 1980. Effects of leaf age and plant life-history on herbivory. Nature 284: 545-46.
20. Coley, P. D. 1990. Tasas de herbivorismo en diferentes árboles tropicales, p. 191-200. In E. G. Leigh Jr., A. S. Rand & D. M. Windsor (eds.). Ecología de un Bosque Tropical: ciclos estacionales y cambios a largo plazo. Instituto Smithsonian de Investigaciones Tropicales, Panama, Panama.
21. Coley, P. D. & J. A. Barone. 1996. Herbivory and plant defenses in tropical forest. Ann. Rev. Ecol. Syst. 27: 305-335.
22. Coley, P. D., & T. A. Kursar. 1996. Anti-herbivore defenses of young tropical leaves: physiological constraints and ecological tradeoffs, p. 305-336. In S. S. Mulkey, R. L. Chazdon & A. P. Smith (eds.). Tropical Forest Plant Ecophysiology. Chapman & Hall, New York, New York, USA.
23. Cunningham, S. A. 1997. Predator control of seed production by a rain forest understory palm. Oikos 79: 282-290.
24. Daubenmire, R. 1972. Phenology and other characteristics of the tropical semideciduous forest in Northwestern Costa Rica. J. Ecol. 60: 147-170.
25. Dirzo, R. 1984. Insect-plant interactions: some ecophysiological consequences of herbivory, p. 209-224. In E. Medina, H. A. Money & C. Vázquez-Yánes (eds.). Physiological ecology of plants of the wet tropics. Dr W. Junk Publishers, Boston, Massachussetts, USA.
26. Dirzo, R. & C. A. Domínguez. 1995. Plant-herbivore interactions in Mesoamerican tropical dry forests, p. 304-325. In S. H. Bullock & H. A. Mooney (eds.). Seasonally dry tropical forests. Cambridge University, Cambridge, England.
27. Edwards, P. J. 1977. Studies of mineral cycling in a montane rain forest in New Guinea. Part 2. The production and disappearance of litter. J. Ecol. 65: 971-972.
28. Filip, V., R. Dirzo, J. M. Maass & J. Sarukhán. 1995. Within and between year variation in the levels of herbivory on the foliage of trees from Mexican deciduous forest. Biotropica 27: 78-86.
29. Frankie, G. W. 1975. Tropical forest phenology and pollinator plant coevolution, p. 192-209. In L. E. Gilbert & P. H. Raven (eds.). Coevolution of animals and plants. University of Texas, Austin, Texas, USA.
30. Frankie, G. W., H. G. Baker & P. A. Opler. 1974. Comparative phenological studies of trees in tropical wet and dry forest in the lowlands of Costa Rica. J. Ecol. 62: 881-919.
31. Frith, C. B. & D. W. Frith. 1985. Seasonality of insect abundance in an Australian upland tropical rain forest. Aust. J. Ecol. 10: 237-248.
32. Fuchs, E. J. 2000. Efecto del aislamiento espacial y fenológico sobre el flujo génico y el éxito reproductivo de Pachira quinata (Bombacaceae). Tesis de maestría, Universidad de Costa Rica, San José. 54 p.
33. Gentry, A. H. 1995. Diversity and floristic composition of neotropical dry forest, p. 146-194. In S. H. Bullok & H. A. Mooney (eds.). Seasonally dry tropical forest. Cambridge University, Cambridge, England.
34. Gentry, A. H. 1974. Flowering phenology and diversity in tropical Bignoniaceae. Biotropica 6: 64-68.
35. Gillespie, T. W. 1999. Life history characteristics and rarity of woody plants in tropical dry forest fragments of Central America. J. Trop. Ecol. 15: 637-649.
36. Greig, N. 1993. Predispersal seed predation on five Piper species in tropical rainforest. Oecologia 93: 412-420.
37. Hartshorn, G. S. 1983. Plants, p. 118-127. In D. H. Janzen (ed.). Costa Rican Natural History. University of Chicago, Chicago, Illinois, USA.
38. Herrera, C. M. 1989. Vertebrate frugivorous and their interaction with invertebrate fruit predators: Supporting evidence from a Costa Rican dry forest. Oikos 54: 185-188.
39. House, S. M. 1992. Population density and fruit set in three dioecious tree species in Australian tropical rain forest. J. Ecol. 80: 57-69.
40. Jackson, P. C., J. Cavalier, G. Goldstein, F. C. Meinzer & N. M. Holbrook. 1995. Partitioning of water resources among plants of lowland tropical forest. Oecologia 101: 197-203.
41. Janzen, D. H. 1967. Synchronization of sexual reproduction of trees within the dry season in Central America. Evolution 21: 620-637.
42. Janzen, D. H. 1970a. Herbivores and the number of tree species in tropical forest. Amer. Nat. 501-28.
43. Janzen, D. H. 1970b. Jacquinia pungens, a heliophile from understory of deciduous forest. Biotropica 2: 112-119.
44. Janzen, D. H. 1971. Seed predation by animals. Ann. Rev. Ecol. Syst. 2: 465-92.
45. Janzen, D. H. 1977a. Intensity of predation on Pithecellobiumsaman (Leguminosae) seeds by Merobruchus columbinus and Stator limbatus (Bruchidae) in Costa Rican deciduous forest. Trop. Ecol. 18: 162-176.
46. Janzen, D. H. 1977b. Why fruits rot, seeds mold, and meet spoils. Amer. Nat. 11: 691-713.
47. Janzen, D. H. 1980. Specificity of seed-attacking beetles in Costa Rican deciduous forest. J. Ecol. 68: 929-952.
48. Janzen, D. H. 1981. Patterns of herbivory in a tropical deciduous forest. Biotropica 13: 271-282.
49. Janzen, D. H. 1983. Jacquinia pungens, p. 265-267. In D. H. Janzen (ed.). Costa Rican Natural History. The University of Chicago, Chicago, Illinois, USA.
50. Janzen, D. H. 1987. Insect diversity of a Costa Rican dry forest: why keep it, and how? Biol. J. Linn. Soc. 30: 343-356.
51. Jonhson, SD & K. E. Steiner. 2000. Generalization versus specialization in plant pollination systems. Tree 15: 140-143.
52. Justiniano, M. J. & T. S. Fredericksen. 2000. Phenology of tree species in Bolivian dry forests. Biotropica 32: 276-281
53. Knudsen, J. T. & B. Ståhl. 1994. Floral odours in the Theophrastaceae. Nord. J. Bot. 22: 259-268.
54. Leopold, A. C. & P. E. Kriedemann. 1975. Plant growth and development. Mc Graw-Hill, New York, New York, USA. 524 p.
55. Lieberman, D. & M. Lieberman. 1984. The causes and consequences of synchronous flushing in a dry tropical forest. Biotropica 16: 193-201.
56. Lowman, M. D. 1984. An assessment of techniques for measuring herbivory: Is rainforest defoliation more intense than we thought? Biotropica 16: 264-268.
57. Maron, J. L. 1998. Insect herbivory above and belowground: individual and joint effects on plant fitness. Ecology 79: 1281-1293.
58. Marquis, R. J. 1984. Leaf herbivores decrease fitness of a tropical plant. Science 226: 537-539.
59. Marquis, R. J. 1988. Phenological variation in the understory shrub Piper arieianum: causes and consequences. Ecology 69: 1552-1565.
60. Marquis, R. J. & H. B. Braker. 1994. Plant-herbivore interactions: diversity, specifity and impact, p. 261-281. In L. A. Mcdade, K. S. Bawa, H. A. Hespenheide & G. S. Hartshorn (eds.). La Selva: Ecology and natural history of a Neotropical Rain Forest. University of Chicago, Chicago, Illinois, USA.
61. Maschinski, J. & T. G. Whitham. 1989. The continuum of plant responses to herbivory: The influence of plant association, nutrient availability, and timing�. Am. Nat. 134:1-19.
62. Mopper, S. & D. Simberloff. 1995. Differential herbivory in an oak population: the role of plant phenology and insect performance. Ecology 76: 1233-1241.
63. Morrison, K. D. & E. G. Reekie. 1995. Pattern of defoliation and its effect on photosynthetic capacity in Oenothera biennis . J. Ecol. 83: 759-767.
64. Morrow, P. A. 1984. Assessing the effects of herbivory, p. 225-231. In E. Medina, H. A. Money & C. Vázquez-Yánes (eds.). Physiological ecology of plants of wet tropics. Dr W. Junk, Boston, Massachussetts, USA.
65. Murcia, C. 2002. Ecología de la polinización, p. 493-530. In M. R. Guariguata & G. H. Kattan (eds.). Ecología y conservación de bosques Neotropicales. LUR, Costa Rica.
66. Murphy, P. G. & A. E. Lugo. 1995. Dry forests of Central America and the Caribbean, p. 9-34. In S. H. Bullok & H. A. Mooney (eds.). Seasonally dry tropical forests. Cambridge University, Cambridge, England.
67. Newstrom, L. E., G. W. Frankie, H. Baker & R. K. Colwell. 1994. Diversity of long term flowering patterns, p. 143-160. In L. A. MacDade, K. S. Bawa, H. A. Hespenheide & G. S. Hartshorn (eds.). La Selva: Ecology and natural history of a Neotropical Rain Forest. University of Chicago, Chicago, Illinois, USA.
68. Oberbauer, S. 1985. Plant water relations of selected species in wet and dry tropical lowland forest in Costa Rica. Rev. Biol. Trop. 33: 137-142.
69. Rathcke, B. & E. P. Lacey. 1985. Phenological patterns of terrestrial plants. Ann. Rev. Ecol. Syst. 16: 179-214.
70. Restrepo, C. 2002. Frugivoría, p. 531-557. In M. R. Guariguata & G. H. Kattan (eds.). Ecología y conservación de bosques neotropicales. LUR, San José, Costa Rica.
71. Richards, A. J. 1997. Plant breeding systems. Chapman & Hall, New York, New York, USA. 529 p.
72. Rivera, G., S. Elliot, L. S. Caldas, G. Nicolossi, V. T. R. Coradin & R. Borchert. 2002. Increasing day-length induces spring flushing of tropical dry forest trees in the absence of rain. Trees 16: 445-456.
73. Roupsard, O., A. Ferhi, A. Granier, F. Pallo, D. Depommier, B. Mallet, H. I. Joly & E. Dreyer. 1999. Reverse phenology and dry season water uptake by Faidherbia albida in an agroforestry parkland of Sudanese West Africa. Funct. Ecol. 13: 460-472.
74. Sallabanks, R. & S. P. Courtney. 1992. Frugivory, seed predation and insect-vertebrate interactions. Ann. Rev. Entomol. 37: 377-400.
75. Smythe, N. 1990. Abundancia estacional de insectos nocturnos en un bosque neotropical, p. 393-402. In E. G. Leigh Jr., A. S. Rand & D. M. Windsor (eds.). Ecología de un bosque tropical: Ciclos estacionales y cambios a largo plazo. Instituto Smithsonian de Investigaciones Tropicales, Panama, Panama.
76. Ståhl, B. 1989. A synopsis of Central American Theophrastaceae. Nord. J. Bot. 9: 15-30.
77. Ståhl, B. 1995. A synopsis of Jacquinia (Theophrastaceae) in the Antilles and South America. Nord. J. Bot. 15: 493-511.
78. Stephenson, A. C. 1981. Flower and fruit abortion: proximate causes and ultimate functions. Ann. Rev. Ecol. Syst. 12: 253-279.
79. Stiles, E. W. 1980. Patterns of fruit presentation and seed dispersal in bird disseminated woody plants in the eastern deciduous forest. Amer. Nat. 116: 670-686.
80. Strauss, S. Y. & W. S. Armbruster. 1997. Linking herbivory and pollination-new perspectives on plant and animal ecology and evolution. Ecology 78:1617-1618.
81. SYSTAT. 1999. SYSTAT version 9. 0 for Windows. SPSS, Chicago, Illinois, USA.
82. Tosi, J. A. 1969. Mapa ecológico, República de Costa Rica: según la clasificación de zonas de vida del mundo de L. R. Holdridge. Centro Científico Tropical, San José.
83. Van Shaik, C. P., J. W. Terborgh & S. J. Wright. 1993. The Phenology of tropical forest: adaptative significance and consequences for primary consumers. Annu. Rev. Ecol. Syst. 24: 353-77.
84. Wheelwright, N. T. 2000. A hypothesis about the timing of flowering fruiting in competing tropical trees, p. 281-283. In N. M. Nadkarni & N. T. Wheelwright (eds.). Monteverde: Ecology and conservation of a tropical cloud forest. Oxford University, Oxford, England. 561 p.
85. Wickens, G. E. 1969. A study of Acacia albida Del. (Mimosoideae). Kew Bulletin 23: 181-202.
86. Wisdom, C. S., C. S. Crawford & E. F. Aldon. 1989. Influence of insect herbivory on photosynthetic area and reproduction in Gutierrezia species. J. Ecol. 77: 685-692.
87. Wolda, H. 1988. Insect seasonality: why? Ann. Rev. Ecol. Syst. 19: 1-18.
88. Wolda, H. 1990. Estacionalidad de los Homoptera de la isla de Barro Colorado, p. 403-414. In E. G. Leigh Jr., A. S. Rand & D. M. Windsor (eds.). Ecología de un bosque tropical: Ciclos estacionales y cambios a largo plazo. Instituto Smithsonian de Investigaciones Tropicales, Panama, Panama.
89. Wright, S. J. & F. H. Cornejo. 1990. Seasonal drought and the leaf fall in tropical forest. Ecology 71: 1165-175.
90. Wright, S. J. 1996. Phenological responses to seasonality in tropical forest plants, p. 440-460. In S. S. Mulkey, R. L. Chazdon & A. P. Smith (eds.). Tropical forest plant ecophysiology. Chapman & Hall, New York, New York, USA.