Small-scale indirect effects determine the outcome of a tripartite plant-disperser-granivore interaction

Oecologia

Volumn 161, Issue 3, 2009, Pages 529-537

  Boulay, Raphaël ^a,b   Carro, Francisco ^a   Soriguer, Ramón C ^a   Cerdá, Xim ^a  

^a DEPARTMENT OF CONSERVATION BIOLOGY   (Spain)

^b UNIVERSITY OF GRANADA   (Spain)

Author keywords

Ant plant mutualism; Indirect effects; Microhabitat; Myrmecochory; Seed dispersal

Indexed keywords

ANT; ANTAGONISM; DICOTYLEDON; GRANIVORY; MICROHABITAT; MUTUALISM; MYRMECOCHORY; PLANT-HERBIVORE INTERACTION; PREDATION RISK; RODENT; SEED PREDATION;

ANIMAL; ANT; ARTICLE; ECOSYSTEM; MURINAE; PHYSIOLOGY; PLANT SEED; SPAIN; STATISTICAL MODEL; SYMBIOSIS; VERATRUM;

ANIMALS; ANTS; ECOSYSTEM; HELLEBORUS; LINEAR MODELS; MURINAE; SEEDS; SPAIN; SYMBIOSIS;

ANIMALIA; APODEMUS SYLVATICUS; FORMICIDAE; HELLEBORUS; HELLEBORUS FOETIDUS; MUS; VERATRUM;

EID: 70349265982     PISSN: 00298549     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00442-009-1404-z     Document Type: Article

References (63)

1. Alcántara JM, Rey PJ, Manzaneda AJ, Boulay R, Ramírez JM, Fedriani JM (2007) Geographic variation in the adaptive landscape for seed size at dispersal of the myrmecochorous Helleborus foetidus. Evol Ecol 21:411-430
2. Andersen AN (1988) Dispersal distance as a benefit of myrmecochory. Oecologia 75:507-511
3. Bas JM, Oliveras J, Goméz C (2009) Myrmecochory and short-term seed fate in Rhamnus alaternus: ant species and seed characteristics A. Oecology (in press)
4. Benkman CW, Holimon WC, Smith JW (2001) The influence of a competitor on the geographic mosaic of coevolution between crossbills and lodgepole pine. Evolution 55:282-294
5. Benkman CW, Parchman TL, Favis A, Siepielski AM (2003) Reciprocal selection causes a coevolutionary arms race between crossbills and lodgepole pine. Am Nat 162:182-194
6. Böhning-Gaese K, Gaese BH, Rabemanatsoa SB (1999) Importance of primary and secondary seed dispersal in the Malagasy tree Comniphora guillaumini. Ecology 80:821-832
7. Boulay R, Fedriani JM, Manzaneda AJ, Cerdá X (2005) Indirect effects of alternative food resources in an ant-plant interaction. Oecologia 144:72-79
8. Boulay R, Coll-Toledano J, Cerdá X (2006) Geographic variations in Helleborus foetidus elaiosome lipid composition: implications for dispersal by ants. Chemoecology 16:1-7
9. Boulay R, Carro F, Soriguer RC, Cerdá X (2007a) Synchrony between fruit maturation and effective dispersers' foraging activity increases seed protection against seed predators. Proc R Soc Lond B 274:2515-2522
10. Boulay R, Cerdá X, Simon T, Roldan M, Hefetz A (2007b) Intraspecific competition in the carpenter ant Camponotus cruentatus: should we expect the Dear Enemy Effect? Anim Behav 74:985-993
11. Bronstein JL (1994) Conditional outcomes in mutualistic interactions. Trends Ecol Evol 9:214-217
12. Carro F, Pérez-Aranda D, Lamosa A, Schmalenberger HP, Pardavila X, Soriguer RC (2007) Indice de capturas y tipo de trampa: ¿qué trampa es para capturar micromamiferos? Galemys 19:73-81
13. Casper BB (1987) Spatial patterns of seed dispersal and postdispersal seed predation of Cryptantha flava (Boraginaceae). Am J Bot 74:1646-1655
14. Cerdá X, Retana J, Cros S (1997) Thermal disruption of transitive hierarchies in Mediterranean ant communities. J Anim Ecol 66:363-374
15. Crawley MJ (2007) The R book. Wiley, New York
16. Detrain C, Tasse O (2000) Seed drops and caches by the harvester ant Messor barbarus: do they contribute to seed dispersal in Mediterranean grasslands? Naturwissenschaften 87:373-376
17. Edut S, Eilam D (2003) Rodents in open space adjust their behavioral response to the different risk levels during barn-owl attack. BMC Ecol 3:1-16
18. Fedriani JM, Boulay R (2006) Foraging by fearful frugivores: combined effects of fruit ripening and predation risk. Funct Ecol 20:1070-1079
19. Fedriani JM, Rey PJ, Garrido JL, Guitián J, Herrera CM, Medrano M, Sánchez-Lafuente AM, Cerdá X (2004) Geographical variation in the potential of mice to constrain an ant-seed dispersal mutualism. Oikos 105:181-191
20. García-Castaño JL, Kollman J, Jordano P (2006) Spatial variation of post-dispersal seed removal by rodents in highland microhabitats of Spain and Switzerland. Seed Sci Res 16:213-222
21. Garrido JL, Rey P, Cerdá X, Herrera C (2002) Geographic variation of diaspore trati of an ant-dispersed plant (Helleborus foetidus): are ant community and diaspore trait correlated. J Ecol 90:446-455
22. Giladi I (2006) Choosing benefits or partners: a review of the evidence for the evolution of myrmecochory. Oikos 112:481-492
23. Gómez C, Espadaler X (1998) Aphaenogaster senilis Mayr (Hymenoptera, Formicidae): a possible parasite in the Myrmecochory of Euphorbia characias. Sociobiology 32:441-450
24. Gorb SN, Gorb E (1999) Dropping rates of elaiosome-bearing seeds during transport by ants (Formica polyctena Foerst.): implications for distance dispersal. Acta Oecol 20:509-518
25. Gorb E, Gorb S (2003) Seed dispersal by ants in a deciduous forest ecosystem. Kluwer, Dordrecht
26. Heithaus ER (1981) Seed predation by rodents on three ant-dispersed plants. Ecology 62:136-145
27. Herre EA, Knowlton N, Mueller U, Rehner S (1999) The evolution of mutualisms: exploring the paths between conflict and cooperation. Trends Ecol Evol 14:49-53
28. Herrera CM (2002) Seed dispersal by vertebrates. In: Herrera CM, Pellmyr O (eds) Plant-animal interactions. Blackwell, Oxford, pp 185-208
29. Howe HF, Smallwood J (1982) Ecology of seed dispersal. Annu Rev Ecol Syst 13:201-228
30. Hughes L, Westoby M (1992) Fate of seeds adapted for dispersal by ants in Australian sclerophyll vegetation. Ecology 73:1285-1299
31. Hulme PE (1994) Post-dispersal seed predation in grassland: its magnitude and sources of variation. J Ecol 82:645-652
32. Hulme PE (1997) Post-dispersal seed predation and the establishment of vertebrate dispersed plants in Mediterranean scrublands. Oecologia 111:91-98
33. Hulme PE, Borelli T (1999) Variability in post-dispersal seed predation in deciduous woodland: relative importance of location, seed species, burial and density. Plant Ecol 145:149-156
34. Janzen DH (1970) Herbivores and the number of tree species in tropical forests. Am Nat 104:501-528
35. Lortie CJ, Ganey DT, Kotler BP (2000) The effects of gerbil foraging on the natural seedbank and consequences on the annual plant community. Oikos 90:399-407
36. Majer JD, Lamont BB (1985) Removal of seed of Grevillea pteridifolia (Proteaceae) by ants. Austr J Bot 33:611-618
37. Manzaneda AJ, Fedriani JM, Rey PJ (2005) Adaptive advantages of myrmecochory: the predator-avoidance hypothesis tested over a wide geographic range. Ecography 28:583-592
38. Manzaneda AJ, Rey P, Boulay R (2007) Geographic and temporal variations in the ant-seed dispersal assemblage of the perennial herb Helleborus foetidus. Biol J Linn Soc 92:135-150
39. Mark S, Olesen JM (1996) Importance of elaiosome size to removal of ant-dispersal seeds. Oecologia 107:95-101
40. Ness JH (2004) Forest edges and fire ants alter the seed shadow of an ant-dispersed plant. Oecologia 138:448-454
41. O'Dowd DJ, Hay ME (1980) Mutualism between harvester ants and a desert ephemeral: seed escape from rodents. Ecology 61:531-540
42. Oberrath R, Böhning-Gaese K (2002) Phenological adaptation of ant-dispersed plants to seasonal variation in ant activity. Ecology 83:1412-1420
43. Ohara M, Higashi S (1987) Interference by ground beetles with the dispersal by ants of seeds of Trillium species (Liliaceae). J Ecol 75:1091-1098
44. Ohkawara K, Higashi S, Ohara M (1996) Effects of ants, ground beetles and the seed-fall patterns on myrmecochory of Erythronium japonicum Decne. (Liliaceae). Oecologia 106:500-506
45. Oliveras J, Gómez C, Bas JM, Espadaler X (2008) Mechanical defence in seeds to avoid predation by a granivorous ant. Naturwissenschaften 95:501-506
46. Pizo MA, Oliveira PS (1998) Interaction between ants and seeds of a nonmyrmecochorous neotropical tree, Cabralea canjerana (Meliaceae), in the Atlantic forest of southeast Brazil. Am J Bot 85:669-674
47. Prinzing A, Dauber J, Hammer EC, Hammouti N, Böhning-Gaese K (2007) Perturbed partners: opposite responses of plant and animal mutualist guilds to inundation disturbances. Oikos 116:1299-1310
48. Retana J, Picó X, Rodrigo A (2004) Dual role of harvesting ants as seed predators and dispersers of a non-myrmechorous mediterranean perennial herb. Oikos 105:377-385
49. Rey PJ, Manzaneda AJ (2007) Geographical variation in the determinants of seed dispersal success of a myrmecochorous herb. J Ecol 95:1381-1393
50. Rodgerson L (1998) Mechanical defense in seeds adapted for ant dispersal. Ecology 79:1669-1677
51. Segraves KA, Althoff DM, Pellmyr O (2005) Limiting cheaters in mutualism: evidence from hybridization between mutualist and cheater yucca moths. Proc R Soc Lond B 272:2195-2201
52. Servigne P, Detrain C (2008) Ant-seed interactions: combined effects of ant and plant species on seed removal patterns. Insect Soc 55:220-230
53. Smallwood J, Culver DC (1979) Colony movements of some North American ants. J Anim Ecol 48:373-382
54. Strauss SY (1991) Indirect effects in community ecology: their definition, study and importance. Trends Ecol Evol 6:206-210
55. Strauss SY, Irwin RE (2004) Ecological and evolutionary consequences of multispecies plant-animal interactions. Annu Rev Ecol Evol Syst 35:435-466
56. Tarborelli PA, Dacar M, Giannoni SM (2003) Effect of plant cover on seed removal by rodents in the Monte Desert (Mendoza, Argentina). Aust Ecol 28:651-657
57. Thompson JN (1994) The coevolutionary process. The University of Chicago Press, Chicago
58. Thompson JN (2005) The geographic mosaic of coevolution. The University of Chicago Press, Chicago
59. Turnbull CL, Culver DC (1983) The timing of seed dispersal in Viola nuttallii: attraction of dispersers and avoidance of predators. Oecologia 59:360-365
60. Valverde T, Silvertown J (1995) Spatial variation in the seed ecology of a woodland herb (Primula vulgaris) in relation to light environment. Funct Ecol 9:942-950
61. Wang BC, Smith TB (2002) Closing the seed dispersal loop. Trends Ecol Evol 17:379-385
62. Yu DW, Wison HB, Pierce NE (2001) An empirical model of species coexistence in a spatially structured environment. Ecology 82:1761-1771
63. Zelikova TJ, Dunn RR, Sanders NJ (2008) Variation in seed dispersal along an elevational gradient in Great Smoky Mountains National Park. Acta Oecol 34:155-162