Skip to main content

Advertisement

SpringerLink
Log in

Could poor seed dispersal contribute to predation by introduced rodents in a Hawaiian dry forest?

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

Dry forests are among the most diverse, yet threatened, communities in Hawai’i. Dry forests throughout the archipelago suffer from a lack of natural regeneration of trees. Two factors that may limit tree recruitment include poor seed dispersal and seed predation by rodents. Poor or limited dispersal of fleshy-fruited species results in seeds and fruits falling directly under parents. Dispersed and non-dispersed seeds may differ in their vulnerability to predation. We tested effects of seed location (under/away from parent trees) and pulp (presence/absence) on predation of four native species that suffer from limited dispersal and one readily-dispersed alien species in Kanaio Natural Area Reserve, Maui. Three natives (Diospyros sandwicensis, Pleomele auwahiensis, Santalum ellipticum), had significantly more seeds removed under parent trees than in exposed sites away from trees. For the one alien (Bocconia frutescens) and two native trees (D. sandwicensis, P. auwahiensis) that were evaluated, significantly more intact fruits were removed than were cleaned seeds. Presence of teeth marks and gnawed seed husk fragments indicate introduced rodents are destroying many of the seeds they remove. These results suggest that seed predation is disproportionately concentrated among poorly-dispersed seeds and may contribute to recruitment failure.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Aide TM, Cavelier J (1994) Barriers to lowland tropical forest restoration in the Sierra Nevada de Santa Marta, Colombia. Restor Ecol 2:219–229

    Article  Google Scholar 

  • Aide TM, Zimmerman JK, Pascarella JB, Rivera L, Marcano-Vega H (2000) Forest regeneration in a chronosequence of tropical abandoned pastures: implications for restoration ecology. Restor Ecol 8:328–338

    Article  Google Scholar 

  • Allen RB, Lee WG, Rance BD (1994) Regeneration in indigenous forest after eradication of Norway rats, Breaksea Island, New Zealand. N Z J Bot 32:429–439

    Google Scholar 

  • Athens JS (2009) Rattus exulans and the catastrophic disappearance of Hawai’i’s native lowland forest. Biol Invasions 11:1489–1501

    Article  Google Scholar 

  • Athens JS, Tuggle HD, Ward JV, Welch DJ (2002) Avifaunal extinctions, vegetation change, and Polynesian impacts in prehistoric Hawai’i. Archaeol Oceania 37:57–78

    Google Scholar 

  • Atkinson IAE (1977) A reassessment of factors, particularly Rattus L., that influenced the decline of endemic forest birds in the Hawaiian Islands. Pac Sci 31:109–133

    Google Scholar 

  • Balcomb SR, Chapman CA (2003) Bridging the gap: influence of seed deposition on seedling recruitment in a primate–tree interaction. Ecol Monogr 73:625–642

    Article  Google Scholar 

  • Bonilla-Moheno M, Holl KD (2009) Direct seeding to restore tropical mature-forest species in areas of slash-and-burn agriculture. Restor Ecol. doi:10.1111/j.1526-100X.2009.00580.x

  • Brooks S, Cordell S, Perry L (2009) Broadcast seeding as a potential tool to reestablish native species in degraded dry forest ecosystems in Hawaii. Ecol Rest 27:300–305

    Article  Google Scholar 

  • Bullock SH (1995) Plant reproduction in neotropical dry forests. In: Bullock SH, Mooney HA, Medina E (eds) Seasonally dry tropical forests. Cambridge University Press, Cambridge, pp 277–303

    Chapter  Google Scholar 

  • Bustamante RO, Simonetti JA (2000) Seed predation and seedling recruitment in plants: the effect of the distance between parents. Plant Ecol 147:173–183

    Article  Google Scholar 

  • Cabin RJ, Weller SG, Lorence DH, Flynn TW, Sakai AK, Sandquist D, Hadway L (2000) Effects of long-term ungulate exclusion and recent non-native species control on the preservation and restoration of a Hawaiian tropical dry forest. Conserv Biol 14:439–453

    Article  Google Scholar 

  • Campbell DJ, Atkinson IAE (2002) Depression of tree recruitment by the Pacific rat (Rattus exulans Peale) on New Zealand’s northern offshore islands. Biol Conserv 107:19–35

    Article  Google Scholar 

  • Campbell DJ, Moller H, Ramsay GW, Watt JC (1984) Observations on foods of kiore (Rattus exulans) found in husking stations on northern offshore islands of New Zealand. N Z J Ecol 7:131–138

    Google Scholar 

  • Chapman CA, Chapman LJ (1996) Frugivory and the fate of dispersed and non-dispersed seeds of six African tree species. J Trop Ecol 12:491–504

    Article  Google Scholar 

  • Chimera CG (2004) Investigating seed dispersal and seed predation in a Hawaiian dry forest community. Unpublished M.Sc. Thesis, University of Hawaii at Manoa, Honolulu

  • Chimera CG, Drake DR (2010) Patterns of seed dispersal and dispersal failure in a Hawaiian dry forest having only introduced birds. Biotropica 42:493–502

    Article  Google Scholar 

  • Choquenot D, Ruscoe WA (2000) Mouse population eruptions in New Zealand forests: the role of population density and seedfall. J Animal Ecol 69:1058–1070

    Article  Google Scholar 

  • Clark DA (1982) Foraging behavior of a vertebrate omnivore (Rattus rattus): meal structure, sampling and diet breadth. Ecology 63:763–772

    Article  Google Scholar 

  • Clark CJ, Paulsen JR, Connor EF, Parker VT (2004) Fruiting trees as dispersal foci in a semi-deciduous tropical forest. Oecologia 139:66–75

    Article  PubMed  CAS  Google Scholar 

  • Cole FR, Loope LL, Medeiros AC, Raikes JA, Wood CS (1995) Conservation implications of introduced game birds in high-elevation Hawaiian shrubland. Conserv Biol 9:306–313

    Article  Google Scholar 

  • Cole FR, Loope LL, Medeiros AC, Howe CE, Anderson LJ (2000) Food habits of introduced rodents in high elevation shrubland of Haleakala National Park, Maui, Hawai’i. Pac Sci 54:313–329

    Google Scholar 

  • Crawley MJ (2001) Seed predators and plant population dynamics. In: Fenner M (ed) Seeds: the ecology of regeneration in plant communities. CABI, Wallingford, pp 167–182

    Google Scholar 

  • Cuddihy LW, Stone CP (1990) Alteration of native Hawaiian vegetation. Cooperative National Park Resources Studies Unit, University of Hawai’i, Honolulu

  • Delgado Garcia JD (2002) Interaction between introduced rats and frugivore bird-plant system in a relict island forest. J Nat Hist 36:1247–1258

    Article  Google Scholar 

  • DeSteven D, Putz FE (1984) Impact of mammals on early recruitment of a tropical canopy tree, Dipteryx panamensis, in Panama. Oikos 43:207–216

    Article  Google Scholar 

  • Drake DR, Hunt TL (2009) Invasive rodents on islands: integrating historical and contemporary ecology. Biol Invasions 11:1483–1487

    Article  Google Scholar 

  • Efford MG, Fitzgerald BM, Karl BJ, Berben PH (2006) Population dynamics of the ship rat Rattus rattus L. in the Orongorongo Valley, New Zealand. N Z J Zool 33:273–297

    Google Scholar 

  • Ferguson RN, Drake DR (1999) Influence of vegetation structure on spatial patterns of seed deposition by birds. N Z J Bot 37:671–677

    Article  Google Scholar 

  • Figueroa JA, Muñoz AA, Mella JE, Arroyo MTK (2002) Pre- and post-dispersal seed predation in a Mediterranean-type climate montane sclerophyllous forest in central Chile. Aust J Bot 50:183–195

    Article  Google Scholar 

  • Giambelluca TW, Nullet MA, Schroder TA (1986) Rainfall atlas of Hawai’i. State of Hawaii, Department of Land and Natural Resources, Division of Water and Land Development, Report R76, Honolulu

  • Gryj EO, Dominguez CA (1996) Fruit removal and postdispersal survivorship in the tropical dry forest shrub Erythroxylum havanense–ecological and evolutionary implications. Oecologia 108:368–374

    Google Scholar 

  • Guariguata MR, Pinard MA (1998) Ecological knowledge of regeneration from seed in neotropical forest trees: implications for natural forest management. For Ecol Manage 112:87–99

    Article  Google Scholar 

  • Hadfield MG, Saufield JE (2009) The demographics of destruction: isolated populations of arboreal snails and sustained predation by rats on the island of Moloka’i 1982–2006. Biol Invasions 11:1595–1609

    Article  Google Scholar 

  • Hadfield MG, Miller SE, Carwile AH (1993) The decimation of endemic Hawai’ian tree snails by alien predators. Am Zool 33(6):610–622

    Google Scholar 

  • Hammond DS (1995) Post-dispersal seed and seedling mortality of tropical dry forest trees after shifting agriculture, Chiapas, Mexico. J Trop Ecol 11:295–313

    Article  Google Scholar 

  • Hau CH (1997) Tree seed predation on degraded hillsides in Hong Kong. For Ecol Manage 99:215–221

    Article  Google Scholar 

  • Hay ME, Fuller PJ (1981) Seed escape from heteromyid rodents: the importance of microhabitat and seed preference. Ecology 62:1395–1399

    Article  Google Scholar 

  • Holl KD (2002) Effect of shrubs on tree seedling establishment in an abandoned tropical pasture. J Ecol 90:179–187

    Article  Google Scholar 

  • Holl KD, Lulow ME (1997) Effects of species, habitat, and distance from edge on post-dispersal seed predation in a tropical rainforest. Biotropica 29:459–468

    Article  Google Scholar 

  • Holl KD, Loik ME, Lin EHV, Samuels IA (2000) Tropical montane forest restoration in Costa Rica: overcoming barriers to dispersal and establishment. Restor Ecol 8:339–349

    Article  Google Scholar 

  • Howe HF, Brown JS (1999) Effects of birds and rodents on synthetic tallgrass communities. Ecology 80:1776–1781

    Article  Google Scholar 

  • Howe HF, Schupp EW, Westley LC (1985) Early consequences of seed dispersal for a neotropical tree (Virola surinamensis). Ecology 66:781–791

    Article  Google Scholar 

  • Hulme PE (1997) Post-dispersal seed predation and the establishment of vertebrate dispersed plants in Mediterranean scrublands. Oecologia 111:91–98

    Article  Google Scholar 

  • Hulme PE (1998) Post-dispersal seed predation: consequences for plant demography and evolution. Perspect Plant Ecol Evol Syst 1:32–46

    Article  Google Scholar 

  • Inglis IR, Shepherd DS, Smith P, Haynes PJ, Bull DS, Cowan DP, Whitehead D (1996) Foraging behavior of wild rats (Rattus norvegicus) towards new foods and bait containers. Appl Anim Behav Sci 47:175–190

    Article  Google Scholar 

  • Janzen DH (1971) Seed predation by animals. Annu Rev Ecol Syst 26:465–492

    Article  Google Scholar 

  • Janzen DH (1988) Tropical dry forests, the most endangered major tropical ecosystem. In: Wilson EO (ed) Biodiversity. National Academy Press, Washington, pp 130–144

    Google Scholar 

  • Jones FA, Peterson CJ, Haines BL (2003) Seed predation in neotropical pre-montane pastures: site, distance and species effects. Biotropica 35:219–225

    Google Scholar 

  • Jordano P, Schupp EW (2000) Seed disperser effectiveness: the quantity component and patterns of seed rain for Prunus mahaleb. Ecol Monogr 70:591–615

    Google Scholar 

  • Kitajima K, Fenner M (2001) Ecology of seedling regeneration. In: Fenner M (ed) Seeds: the ecology of regeneration in plant communities. CABI, Wallingford, pp 331–359

    Google Scholar 

  • Loope LL (1998) Hawai’i and the Pacific Islands. In: Mac MJ, Opler PA, Puckett Haecker CE, Doran PD (eds) Status and trends of the nation’s biological resources. US Geological Survey, Reston, pp 747–774

    Google Scholar 

  • McConkey KR, Drake DR, Meehan HJ, Parsons N (2003) Husking stations provide evidence of seed predation by introduced rodents in Tongan rain forests. Biol Conserv 109:221–225

    Article  Google Scholar 

  • McDonnell MJ, Stiles EW (1983) The structural complexity of old field vegetation and the recruitment of bird-dispersed plant species. Oecologia 56:109–116

    Article  Google Scholar 

  • Medeiros AC (2004) Phenology, reproductive potential, seed dispersal and predation, and seedling establishment of three invasive plant species in a Hawaiian rainforest. PhD dissertation, University of Hawaii at Manoa, Honolulu, Hawaii

  • Medeiros AC, Loope LL, Holt RA (1986) Status of native flowering plant species on the south slope of Haleakala, East Maui, Hawaii. University of Hawaii Cooperative National Park Resource Studies Unit Technical Report 59, Honolulu

  • Mehrhoff LA (1998) Endangered and threatened species. In: Juvik SP, Juvik JO (eds) Atlas of Hawaii, 3rd edn. University of Hawaii Press, Honolulu, pp 150–153

    Google Scholar 

  • Meyer J-Y (2004) Threat of invasive alien plants to native flora and forest vegetation of eastern Polynesia. Pac Sci 58:357–375

    Article  Google Scholar 

  • Meyer J-Y, Butaud J-F (2009) The impacts of rats on the endangered native flora of French Polynesia (Pacific Islands): drivers of plant extinction or coup de grâce species? Biol Invasions 11:1569–1585

    Article  Google Scholar 

  • Meyer J-Y, Florence J (1996) Tahiti’s native flora endangered by the invasion of Miconia calvescens DC. (Melastomataceae). J Biogeogr 23:775–781

    Article  Google Scholar 

  • Minitab Inc (2007) Minitab for Windows Release 15.1.30.0 State College, PA

  • Moles AT, Drake DR (1999) Post-dispersal seed predation on eleven large-seeded species from the New Zealand flora: a preliminary study in secondary forest. N Z J Bot 37:679–685

    Article  Google Scholar 

  • Mueller-Dombois D, Fosberg FR (1998) Vegetation of the tropical Pacific islands. Springer, New York

    Google Scholar 

  • Murúa R, González L (1982) Microhabitat selection by two Chilean cricetid rodents. Oecologia 52:12–15

    Article  Google Scholar 

  • Nuñez MA, Simberloff D, Relva MA (2008) Seed predation as a barrier to alien conifer invasions. Biol Invasions 10:1389–1398

    Article  Google Scholar 

  • Nystrand O, Granstrom A (1997) Post-dispersal predation on Pinus sylvestris seeds by Fringilla spp: ground substrate affects selection for seed color. Oecologia 110:353–359

    Article  Google Scholar 

  • Pau S, Gillespie TW, Price JP (2009) Natural history, biogeography, and endangerment of Hawaiian dry forest trees. Biodivers Conserv 18:3167–3182

    Article  Google Scholar 

  • Perez HE, Shiels AB, Zaleski HM, Drake DR (2008) Germination after simulated rat damage in seeds of two endemic Hawaiian palm species. J Trop Ecol 24:555–558

    Article  Google Scholar 

  • Pratt HD, Bruner PL, Berrett DG (1987) The birds of Hawai’i and the tropical Pacific. Princeton University Press, Princeton

    Google Scholar 

  • Pratt TK, Atkinson CT, Banko PC, Jacobi JD, Woodworth BL (2009) Conservation biology of Hawaiian forest birds: implications for island avifauna. Yale University Press, New Haven

    Google Scholar 

  • Ramón Obeso J, Fernández-Calvo IC (2002) Fruit removal, pyrene dispersal, post-dispersal predation and seedling establishment of a bird-dispersed species. Plant Ecol 165:223–233

    Article  Google Scholar 

  • Ryan B, Joiner BL (2001) Minitab handbook, 4th edn. Duxbury Press, Pacific Grove

    Google Scholar 

  • Sánchez-Cordeiro V, Martínez-Gallardo R (1998) Postdispersal fruit and seed removal by forest-dwelling rodents in a lowland rainforest in Mexico. J Trop Ecol 14:139–151

    Article  Google Scholar 

  • Scott JM, Mountainspring S, Ramsey FL, Kepler CB (1986) Forest bird communities of the Hawaiian Island: their dynamics, ecology, and conservation. Studies in Avian Biology 9. Cooper Ornithological Society, Los Angeles

    Google Scholar 

  • Shiels AB (2010) Frugivory by introduced black rats (Rattus rattus) promotes dispersal of invasive plant seeds. Biol Invasions (in press) doi:10.1007/s10530-010-9868-7

  • Shiels AB, Drake DR (2010) Are introduced rats (Rattus rattus) both seed predators and dispersers in Hawaii? Biol Invasions (in press) doi:10.1007/s10530-010-9876-7

  • Shiels AB, Walker LR (2003) Bird perches increase forest seeds on Puerto Rican landslides. Restor Ecol 11:457–465

    Article  Google Scholar 

  • Stiles EW (2001) Animals as seed dispersers. In: Fenner M (ed) Seeds: the ecology of regeneration in plant communities. CABI, Wallingford, pp 111–124

    Google Scholar 

  • Stone CP (1985) Non-native animals in Hawai’i’s native ecosystems: toward controlling the adverse effects of introduced vertebrates. In: Stone CP, Scott M (eds) Hawai’i’s terrestrial ecosystems: preservation and management. Cooperative National Park Resources Studies Unit. University of Hawai’i, Honolulu, pp 251–297

    Google Scholar 

  • Sugihara RT (1997) Abundance and diets of rats in two native Hawaiian forests. Pac Sci 51:189–198

    Google Scholar 

  • Terborgh J, Loso E, Riley MP, Filey MB (1993) Predation by vertebrates and invertebrates on the seeds of five canopy tree species of an Amazonian forest. In: Fleming TH, Estrada A (eds) Frugivory and seed dispersal: ecological and evolutionary aspects. Kluwer Academic Publishers, Belgium, pp 375–386

    Google Scholar 

  • Tomich PQ (1962) Notes on the barn owl in Hawai’i. Elepaio 23:16–17

    Google Scholar 

  • Tomich PQ (1986) Mammals in Hawaii, 2nd edn. Bishop Museum Press, Honolulu

    Google Scholar 

  • Towns DR, Atkinson IAE, Daugherty CH (2006) Have the harmful effects of introduced rats on islands been exaggerated? Biol Invasions 8:863–891

    Article  Google Scholar 

  • Traveset A, Richardson DM (2006) Biological invasions as disruptors of plant reproductive mutualisms. Trends Ecol Evol 21:208–216

    Article  PubMed  Google Scholar 

  • Traveset A, Nogales M, Alcover JA, Delgado JD, López-Darias M, Godoy D, Igual JM, Bover P (2009) A review on the effects of alien rodents in the Balearic (Western Mediterranean Sea) and Canary Islands (Eastern Atlantic Ocean). Biol Invasions 11:1653–1670

    Article  Google Scholar 

  • Uhl C (1998) Restoration of degraded lands in the Amazon basin. In: Wilson EO (ed) Biodiversity. National Academy Press, Washington, pp 326–332

    Google Scholar 

  • Vander Wall SB (2009) How rodents smell buried seeds: a model based on the behavior of pesticides in soil. J Mammal 84:1089–1099

    Article  Google Scholar 

  • Vander Wall SB, Longland WS (2004) Diplochory: are two seed dispersers better than one? Trends Ecol Evol 19:155–161

    Article  PubMed  Google Scholar 

  • Vander Wall SB, Kuhn KM, Beck MJ (2005) Seed removal, seed predation, and secondary dispersal. Ecology 86:801–806

    Article  Google Scholar 

  • Wagner WL, Herbst DR, Sohmer SH (1999) Manual of the flowering plants of Hawai’i, vol 2. Bishop Museum special publication 83. University of Hawaii Press, Honolulu

    Google Scholar 

  • Wenny DG (2000) Seed dispersal, seed predation, and seedling recruitment of a neotropical montane tree. Ecol Monogr 70:331–351

    Article  Google Scholar 

  • Wijdeven SMJ, Kuzee ME (2000) Seed availability as a limiting factor in forest recovery processes in Costa Rica. Restor Ecol 8:414–424

    Article  Google Scholar 

  • Williams PA, Karl BJ, Bannister P, Lee WG (2000) Small mammals as potential seed dispersers in New Zealand. Austral Ecol 25:523–532

    Article  Google Scholar 

  • Zar JH (1999) Biostatistical analysis, 4th edn. Prentice Hall, New Jersey

    Google Scholar 

  • Ziegler AC (2002) Hawaiian natural history, ecology and evolution. University of Hawaii Press, Honolulu

    Google Scholar 

  • Zimmerman JK, Pascarella JB, Aide TM (2000) Barriers to forest regeneration in an abandoned pasture in Puerto Rico. Restor Ecol 8:350–360

    Article  Google Scholar 

Download references

Acknowledgments

We thank Sumner Erdman and the office staff of Ulupalakua Ranch, and Betsy Gagne, Bill Evanson and Bryon Stevens (Hawaii Natural Area Reserve System) for providing permits and access to the study site. We thank Lloyd Loope and Art Medeiros for providing technical advice and logistical support. We thank Gerry Carr, Dave Duffy, Aaron Shiels, Jean-Yves Meyer, Chris Buddenhagen, Marc Cadotte, and the anonymous reviewers for providing comments on the manuscript. We thank the Ecology, Evolution and Conservation Biology Program, the Hawaii Audubon Society, the Dai Ho Chun Fellowship, and the Charles H. Lamoureux Fellowship in Plant Conservation for providing funding.

Author information

Authors and Affiliations

  1. Botany Department and Pacific Cooperative Studies Unit, University of Hawaii, P.O. Box 1502, Makawao, HI, 96768, USA

    Charles G. Chimera

  2. Botany Department, University of Hawaii, Honolulu, HI, 96922, USA

    Donald R. Drake

Authors
  1. Charles G. Chimera
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Donald R. Drake
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Charles G. Chimera.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Chimera, C.G., Drake, D.R. Could poor seed dispersal contribute to predation by introduced rodents in a Hawaiian dry forest?. Biol Invasions 13, 1029–1042 (2011). https://doi.org/10.1007/s10530-010-9887-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-010-9887-4

Keywords

Search

Navigation