, Volume 79, Issue 3, pp 417–426

Scatter-and clump-dispersal and seedling demography: hypothesis and implications

  • Henry F. Howe


Fruit-eating animals deposit viable seeds in patterns that determine the conditions under which seeds and seedlings live or die. Many tree species are scatter-dispersed by birds, bats, or other small frugivores that regurgitate, defecate, or drop seeds singly or in pairs. These scatterdispersed plant species normally recruit as isolated individuals, and are unlikely to evolve exceptional resistance to herbivores, pathogens, or to other sources of density-dependent seed or seedling mortality. Other tree species are clump-dispersed by larger terrestrial or arboreal frugivores that defecate seeds in masses which produce bouquets of seedlings. Because their seeds invariably germinate in close proximity to other seedlings, clump-dispersed species necessarily evolve chemical or mechanical defenses against seed predators, pathogens, and herbivores that act in a densitydependent manner.

Population and genetic attributes should reflect this basic dichotomy in the conditions of seedling recruitment. I predict that seedlings of scatter-dispersed species rarely survive near parents or in dense aggregations under frugivore roosts. Seed dispersal should be mandatory, often to light gaps or other special habitats. Outbred adults and juveniles are expected to exist at low densities in loose aggregations or random distributions. Seedlings of clump-dispersed trees are pre-adapted for survival in dense aggregations near parents, as well as in fecal clumps. Substantial recruitment of juveniles and young adults should occur from undispersed seeds under and near parent trees. Such species should be common, highly aggregated, and show strong genetic family structure. Because recruitment requires dispersal, scatter-dispersed plant species should be especially vulnerable to loss of dispersal agents. Because offspring consistently recruit near parents, clump-dispersed plants should be less vulnerable to temporary loss of dispersal agents.

Key words

Demography Ecology Frugivory Seed dispersal Tropics 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Alexandre DY (1978) Le role disseminateur des elephants en foret de tal, Cote-D'Ivoire. Terre et Vie 32:47–71Google Scholar
  2. Augspurger CK (1983a) Offspring recuitment around tropical trees: changes in cohort distance with time. Oikos 40:189–196CrossRefGoogle Scholar
  3. Augspurger CK (1983b) Seed dispersal of the tropical tree, Platypodium elegans, and the escape of its seedlings from fungal pathogens. J Ecol 71:759–772CrossRefGoogle Scholar
  4. Augspurger CK (1984) Seedling survival of tropical tree species: interactions of dispersal distance, light-gaps, and pathogens. Ecology 65:1705–1712CrossRefGoogle Scholar
  5. Augspurger CK, Kelly CK (1984) Pathogen mortality of tropical tree seedlings: experimental studies of the effects of dispersal distance, seedling density, and light conditions. Oecologia 61:211–217CrossRefGoogle Scholar
  6. Bawa KS (1974) Breeding systems of tree species of a lowland tropical community. Evolution 28:85–92CrossRefGoogle Scholar
  7. Bawa KS (1980) Evolution of dioecy in flowering plants. Ann Rev Ecol Syst 11:15–39CrossRefGoogle Scholar
  8. Bawa KS, Perry DR, Beach JH (1985) Reproductive biology of tropical lowland rain forest trees. I. Sexual systems and incompatibility mechanisms. Am J Bot 72:331–345CrossRefGoogle Scholar
  9. Becker P, Wong M (1985) Seed dispersal, seed predation, and juvenile mortality of Aglaia sp. (Meliaceae) in lowland Dipterocarp rainforest. Biotropica 17:230–237CrossRefGoogle Scholar
  10. Becker P, Lee LW, Rothman ED, Hamilton WD (1985) Seed predation and the coexistence of tree species: Hubbell's models revisited. Oikos 44:382–390CrossRefGoogle Scholar
  11. Bonaccorso FJ (1979) Foraging and reproductive ecology in a Panamanian bat community. Bull Florida State Mus Biol Sci Vol 24:359–408Google Scholar
  12. Charles-Dominique P (1986) Inter-relations between frugivorous vertebrates and pioneer plants: Cecropia, birds and bats in French Guyana. In: Estrada A, Fleming TH (eds) Frugivores and seed dispersal: 119–135. Dr. W. Junk Publishers, DordrechtCrossRefGoogle Scholar
  13. Clark DA, Clark DB (1984) Spacing dynamics of a tropical rain forest trees: evaluation of the Janzen-Connell model. Am Nat 124:769–788CrossRefGoogle Scholar
  14. Connell JH (1971) On the role of natural enemies in preventing competitive exclusion in some marine animals and in rain forest trees. In: PJ Den Boer, PR Gradwell (eds) Dynamics of populations: 298–312. Wageningen, NetherlandsGoogle Scholar
  15. Davidar P (1983) Birds and neotropical mistletoes: effects on seedling recruitment. Oecologia 60:271–273CrossRefGoogle Scholar
  16. De Steven D, Putz F (1984) Impact of mammals on early recruitment of a tropical canopy tree, Dipteryx panamensis, in Panama. Oikos 43:207–216CrossRefGoogle Scholar
  17. Dinerstein E, Wemmer CM (1988) Fruits Rhinoceros eat: Megagaunal seed dispersal on a South Asian flood plain. Ecology 69:1768–1775CrossRefGoogle Scholar
  18. Dirzo R, Dominguez CA (1986) Seed shadows, seed predation and the advantages of dispersal. In: Estrada A and Fleming TH (eds). Frugivory and seed dispersal: 237–249. Dr. W. Junk Publishers, DordrechtCrossRefGoogle Scholar
  19. Dubost G (1984) Comparison of the diets of frugivorous forest ruminants of Gabon. J Mammalogy 65:298–316CrossRefGoogle Scholar
  20. Estrada A, Coates-Estrada R (1986) Frugivory in howling monkeys (Alouatta palliata) at Los Tuxtlas, Mexico: dispersal and the fate of seeds. In: A Estrada and TH Fleming (eds). Frugivores and seed dispersal: 93–105. Dr. W. Junk Publishers, DordrechtCrossRefGoogle Scholar
  21. Fleming TH, Heithaus ER (1981) Frugivorous bats, seed shadows and the structure of tropical forests. Biotropica [Suppl] 13:45–53CrossRefGoogle Scholar
  22. Frankie GW, Baker HG, Opler PA (1974) Comparative phenological studies of trees in tropical wet and dry forests in the lowlands of Costa Rica. J Ecol 62:881–919CrossRefGoogle Scholar
  23. Garwood NC (1983) Seed germination in a seasonal tropical forest in Panama: a community approach. Ecol Monogr 53:159–181CrossRefGoogle Scholar
  24. Gautier-Hion A, Emmons LH, Dubost G (1980) A comparison of the diets of three major groups of primary consumers of Gabon (prinmates, squirrels and ruminants). Oecologia 45:182–189CrossRefGoogle Scholar
  25. Gautier-Hion A, Duplantier J-M, Quris R, Feer F, Sourd C, Decoux J-P, Dubost G, Emmons L, Erard C, Hecketsweiler P, Moungazi A, Roussilhon C, Thiollay J-M (1985) Fruit characters as a basis of fruit choice and seed dispersal in a tropical forest vertebrate community. Oecologia 65:324–337CrossRefGoogle Scholar
  26. Gilbert LE (1980) Food web organization and the conservation of neotropical diversity. In: Soule ME, Wilcox BA (eds) Conservation biology: An evolutionary-ecological perspective: 11–33. Sinauer Associates, Sunderland, MassGoogle Scholar
  27. Greenberg R (1981) Frugivory in some migrant tropical forest wood warblers. Biotropica 13:215–223CrossRefGoogle Scholar
  28. Grime JP (1977) Plant strategies and vegetations processes. Chichester, WileyGoogle Scholar
  29. Grubb PJ (1977) The maintenance of species richness in plant communities. The importance of the regeneration niche. Biol Rev 52:107–145CrossRefGoogle Scholar
  30. Hamrick JL, Loveless MD (1986) The influence of seed dispersal mechanisms on the genetic structure of plant population. In: Estrada A, Fleming TH (eds) Frugivores and seed dispersal: 211–223. Dr. W. Junk Publishers, DordrechtCrossRefGoogle Scholar
  31. Heithaus ER (1982) Coevolution between bats and plants. In: Kunz TH (ed) Ecology of bats. Plenum Press, New York, pp 327–367CrossRefGoogle Scholar
  32. Herrera CM (1982) Seasonal variation in the quality of fruits and diffuse coevolution between plants and avian dispersers. Ecology 63:773–785CrossRefGoogle Scholar
  33. Herrera CM (1984a) Adaptation to frugivory of Mediterranean avian seed dispersers. Ecology 65:609–617CrossRefGoogle Scholar
  34. Herrera CM (1984b) A study of avian frugivores, bird-dispersed plants, and their interaction in Mediterranean scrublands. Ecol Monogr 54:1–23CrossRefGoogle Scholar
  35. Herrera CM (1985) Determinants of plant-animal coevolution: the case of mutualistic vertebrate seed dispersal systems. Oikos 44:132–141CrossRefGoogle Scholar
  36. Howe HF (1977) Bird activity and seed dispersal of a tropical wet forest tree. Ecology 58:539–550CrossRefGoogle Scholar
  37. Howe HF (1979) Feat and frugivory. Amer Nat 114:925–931CrossRefGoogle Scholar
  38. Howe HF (1980) Monkey dispersal and waste of a neotropical tree. Ecology 61:944–959CrossRefGoogle Scholar
  39. Howe HF (1981) Dispersal of a neotropical nutmeg (Virola sebifera) by birds. Auk 98:88–98Google Scholar
  40. Howe HF (1983) Annual variation in a neotropical seed-dispersal system. In: Sutton SL, Whitmore TC, Chadwick AC (eds) Tropical rain forest: ecology and management: 211–227. Blackwell Scientific, OxfordGoogle Scholar
  41. Howe HF (1984b) Implications of seed dispersal by animals for the management of tropical reserves. Biol Conservation 30:261–281CrossRefGoogle Scholar
  42. Howe HF (1984b) Constraints on the evolution of mutualisms. Am Nat 123:764–777CrossRefGoogle Scholar
  43. Howe HF (1985) Gomphothere fruits: a critique. Am Nat 125:853–865CrossRefGoogle Scholar
  44. Howe HF (1986a) Seed dispersal by fruit-eating birds and mammals. In: Murray DR (ed) Seed dispersal: 123–190. Academic Press, SydneyGoogle Scholar
  45. Howe HF (1986b) Consequences of seed dispersal by birds: a case study from Central America. J Bombay Nat Hist Soc [Suppl] 83:19–42Google Scholar
  46. Howe HF (1989) Seed dispersal by birds and mammals: implications for seedling demography.Google Scholar
  47. Howe HF, Estabrook GF (1977) On intraspecific competition for avian dispersers in tropical trees. Am Nat 111:817–832CrossRefGoogle Scholar
  48. Howe HF, Primack R (1975) Differential seed dispersal by birds of the tree Casearia nitida (Flacourtiacease). Biotropica 7:278–283CrossRefGoogle Scholar
  49. Howe HF, Smallwood J (1982) Ecology of seed dispersal. Ann Rev Ecol Syst 13:201–228CrossRefGoogle Scholar
  50. Howe HF, Vande Kerckhove GA (1979) Fecundity and seed dispersal of a tropical tree. Ecology 60:180–189CrossRefGoogle Scholar
  51. Howe HF, Westley LC (1988) Ecological relationships of plants and animals. Oxford University Press, New YorkGoogle Scholar
  52. Howe HF, Schupp EW, Westley LC (1985) Early consequences of seed dispersal for a neotropical tree (Virola surinamensis). Ecology 66:781–791CrossRefGoogle Scholar
  53. Hubbell SP (1979) Tree dispersion, abundance, and diversity in a tropical dry forest. Science 203:1299–1309PubMedCrossRefGoogle Scholar
  54. Hubbell SP (1980) Seed predation and the coexistence of tree species in tropical forests. Oikos 35:214–229CrossRefGoogle Scholar
  55. Hubbell SP, Foster R (1983) Diversity of canopy trees in a neotropical forest and implications for conservation. In: Sutton SL, Whitmore TC, Chadwick A (eds) The tropical rain forest: ecology and management: 25–41. Blackwell Scientific, OxfordGoogle Scholar
  56. Janson C (1983) Adaptation of fruit morphology to dispersal agents in a neotropical forest. Science 219:187–189PubMedCrossRefGoogle Scholar
  57. Janzen DH (1970) Herbivores and the number of tree species in tropical forests. Am Nat 104:501–528CrossRefGoogle Scholar
  58. Janzen DH (1981) Digestive seed predation by a Costa Rican Baird's tapir. Biotropica [Suppl] 13:59–63CrossRefGoogle Scholar
  59. Janzen DH (1982a) Differential seed survival and passage rates in cows and horses, surrogate Pleistocene dispersal agents. Oikos 38:150–156CrossRefGoogle Scholar
  60. Janzen DH (1982b) Removal of seeds from horse dung by tropical rodents: influence of habitat and amount of dung. Ecology 62:1887–1900CrossRefGoogle Scholar
  61. Janzen DH (1986) Mice, big mammals, and seeds: it matters who defecaates what where. In: Estrada A, Fleming TH (eds), Frugivores and seed dispersal: 251–272. Dr. W. Junk Publishers, DordrechtCrossRefGoogle Scholar
  62. Jansen DH, Martin P (1982) Neotropical anachronisms: what the gomphotheres ate. Science 215:19–27CrossRefGoogle Scholar
  63. Janzen DH, Miller GA, Hackforth-Jones J, Poud CM, Hooper K, Janos DP (1976) Two Costa Rican bat-generated seed shadows of Andira inermis (Leguminosae). Ecology 57:1068–1075CrossRefGoogle Scholar
  64. Leigh G, Rand AS, Windsor DS (eds) (1982) The ecology of a tropical forest: seasonal rhythms and long-term changes. Smithsonian Press, Washington, D.C.Google Scholar
  65. Levey DJ (1987) Seed size and fruit-handling techniques of avian frugivores. Am Nat 129:471–485CrossRefGoogle Scholar
  66. Levin D, Kerster H (1974) Gene flow in seed plants. Evol Biol 7:139–220CrossRefGoogle Scholar
  67. Lieberman M, Lieberman D (1986) An experimental study of seed ingestion and germination in a plant-animal assemblage in Ghana. J Trop Ecol 2:113–126CrossRefGoogle Scholar
  68. Lieberman D, Lieberman M, Martin C (1987) Notes on seeds in elephant dung from Bia National Park, Ghana. Biotropica 19:365–369CrossRefGoogle Scholar
  69. Loveless MD, Hamrick JL (1984) Ecological determinants of genetic structure in plant populations. Ann Rev Ecol Syst 15:65–96CrossRefGoogle Scholar
  70. Martin TE (1985) Resource selection by tropical frugivorous birds: integrating multiple interactions. Oecologia 66:563–573CrossRefGoogle Scholar
  71. Martinez-Ramos M, Alvarez-Buylla E (1986) Seed dispersal, gap dynamics, and tree recruitment: the case of Cecropia obtusifolia at Los Tuxtlas, Mexico. In: Estrada A, Fleming TH (eds) Frugivores and seed dispersal: 333–346. Dr. W. Junk Publishers, DordrecletCrossRefGoogle Scholar
  72. McKey D (1975) The ecology of coevolved seed dispersal systems. In: Gilbert LE, Raven PH (eds) Coevolution of animals and plants. U Texas Press, Austin, pp 159–191Google Scholar
  73. Moermond T, Denslow JS (1985) Neotropical avian frugivores: patterns of behavior, morphology, and nutrition with consequences for fruit selection. In: Buckley PA, Foster MS, Morton ES, Ridgely RS, Smith NG (eds) Ornithological 36: 865–897Google Scholar
  74. Moermond T, Denslow JS, Levey DJ, Santana CE (1986) The influence of morphology on fruit choice in neotropical birds. In: Estrada A, Fleming TH (eds) Frugiyores and seed dispersal: 1377–1346. Dr. W. Junk Publishers, The HagueGoogle Scholar
  75. Morrison D (1978a) Lunar phobia in a neotropical fruit bat, Artibeus jamaicensis (Diroptera: Phyllostomatidae). Anim Behav 26:852–855CrossRefGoogle Scholar
  76. Morrison D (1978b) Foraging ecology and energetics of the frugivorous bat Artibeus jamaicensis. Ecology 59:716–723CrossRefGoogle Scholar
  77. Noble JC (1975) The effects of emus (Dromaius novae-hollandiae Latham) on the distribution of the nitre bush (Nitraria billardieri DC). J Ecol 63:979–984CrossRefGoogle Scholar
  78. Reid N (1989) Dispersal of a mistletoe by a honeyeater and a flowerpecker: the components of seed dispersal quality. Ecology 70:137–145CrossRefGoogle Scholar
  79. Schupp EW (1988a) Predation on seeds and early seedlings in the forest understory and in treefall gaps. Oikos 51:71–78CrossRefGoogle Scholar
  80. Schupp EW (1988b) Factors affecting post-dispersal seed survival in a tropical forest. Oecologia 76:525–530Google Scholar
  81. Schupp EW, Howe HF, Augspurger CK, Levey DJ (1989) Arrival and survival in tropical treefall gaps. Ecology (in press)Google Scholar
  82. Smythe N (1986) Competition and resource partitioning in the guild of neotropical terrestrial frugivorous mammals. Ann Rev Ecol Syst 17:169–188CrossRefGoogle Scholar
  83. Sork VL (1985) Germination response in a large-seeded neotropical tree species, Gustavia superba (Lecythidaceae). Biotropica 17:130–136CrossRefGoogle Scholar
  84. Sork V (1987) Effect of predation and light on seedling establishment in Gustavia superba. Ecology 68:1341–1350CrossRefGoogle Scholar
  85. Stocker GC, Irvine AK (1983) Seed dispersal by cassowaries (Casuarius casuarius) in North Queensland's rainforests. Biotropica 15:170–176CrossRefGoogle Scholar
  86. Temple S (1977) Plant-animal mutualism: coevolution with dodo leads to near extinction of plant. Science 203:885–886CrossRefGoogle Scholar
  87. Terborgh J (1983) Five new world primates. Princeton University Press, PrincetonGoogle Scholar
  88. Tomback DF (1983) Nutcrackers and pines: coevolution or coadaptation? In: Nitecki MH (ed). Coevolution: 179–223. University of Chicago Press, ChicagoGoogle Scholar
  89. Van der Pijl L (1972) Principles of dispersal in higher plants. Springer, Berlin Heidelberg New YorkCrossRefGoogle Scholar
  90. Vásquez-Yanes C, Orozco-Segovia A (1986) Dispersal of seeds by animals: effect of light-controlled dormancy in Cecropia obtusifolia. In: Estrada A, Fleming TH (eds) Frugivores and seed dispersal: 71–78. Dr. W. Junk Publishers, DordrechtCrossRefGoogle Scholar
  91. Whellwright N (1985) Fruit size, gape width, and the diets of fruit-eating birds. Ecology 66:808–818CrossRefGoogle Scholar
  92. Whitmore TC (1984) Tropical rain forests of the Far East. Oxford University Press, LondonGoogle Scholar
  93. Wright SJ (1983) The dispersion of eggs by a bruchid beetle among Scheelea palm seeds and the effect of distance to the parent palm. Ecology 64:1016–1021CrossRefGoogle Scholar
  94. Wright SJ, Howe HF (1987) Spatial pattern and mortality in Colorado desert perennials. Oecologia 73:543–552CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 1989

Authors and Affiliations

  • Henry F. Howe
    • 1
  1. 1.Department of Biological SciencesUniversity of Illinois at ChicagoChicagoUSA

Personalised recommendations