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The role of avian frugivores in germination of seeds of fleshy-fruited invasive alien plants

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Abstract

Many highly invasive plant species have fleshy fruits which are eaten by native frugivorous animals. These frugivores play an important role in long-distance seed dispersal, and may also affect germination success. The aim of this study was to determine whether generalist frugivores enhance or decrease seed germination of invasive alien species through pulp removal or seed coat abrasion, besides serving as dispersal agents. Fruits of four fleshy-fruited invasive alien plant species, namely Solanum mauritianum, Cinnamomum camphora, Lantana camara and Psidium guajava, were fed to three generalist avian frugivorous species, which have been observed feeding on these fruits in the wild. Seed retention time was recorded as this affects dispersal distance and the duration that seeds are exposed to the effects of the gut. Seeds removed from excreta, seeds from manually de-pulped fruit, and whole fruit were planted in soil trays housed in a greenhouse. Daily germination counts were done. Seed retention times differed significantly between bird species for all fruits, except those of C. camphora. However, all frugivores had a similar effect on the germination success of seeds of S. mauritianum, L. camara and P. guajava, showing that gut retention time was not important. Germination of seeds from manually de-pulped fruits did not differ from that of ingested seeds of all plant species, suggesting that seed coat abrasion was also not important. Pulp removal resulted in significantly higher germination rates, both in the two species with larger, multi-seeded fruit (S. mauritianum and P. guajava), and in the two species having single-seeded fruit with waxy exocarps (C. camphora and L. camara). Pulp removal also resulted in significantly earlier germination of L. camara and P. guajava seeds. Therefore, frugivores not only accelerate dispersal, but also greatly enhance seed germination of all fleshy-fruited invasive alien species in this study.

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References

  • Abul-Fatih HA, Bazzaz FA (1979) The biology of Ambrosia trifida L. II. Germination, emergence, growth and survival. New Phytol 83:817–827

    Article  Google Scholar 

  • Adsule RN, Kadam SS (1995) Guava. In: Salunkhe D, Kadam S (eds) Handbook of fruit science and technology: production, composition, storage, and processing. Marcel Dekker Inc., New York, pp 419–433

    Google Scholar 

  • Agami M, Waisel Y (1988) The role of fish in distribution and germination of seeds of the submerged macrophytes Najas marina L. and Ruppia maritima L. Oecologia 76:83–88

    Google Scholar 

  • Barnea A, Yomtov Y, Friedman J (1990) Differential germination of two closely related species of Solanum in response to bird ingestion. Oikos 57:222–228

    Article  Google Scholar 

  • Barnea A, Yomtov Y, Friedman J (1991) Does ingestion by birds affect seed-germination. Funct Ecol 5:394–402

    Article  Google Scholar 

  • Bartuszevige AM, Gorchov DL (2006) Avian seed dispersal of an invasive shrub. Biol Invasions 8:1013–1022

    Article  Google Scholar 

  • Bass DA (1990) Dispersal of an introduced shrub (Crataegus monogyna) by the brush-tailed Possum (Trichosurus vulpecula). Aust J Ecol 15:227–229

    Article  Google Scholar 

  • Berens DG, Farwig N, Schaab G, Boehning-Gaese K (2008) Exotic guavas are foci of forest regeneration in Kenyan farmland. Biotropica 40:104–112

    Google Scholar 

  • Buchanan R (1989) Pied Currawongs (Strepera graculina): their diet and role in weed dispersal in suburban Sydney, New South Wales. Proc Linn Soc NSW 111:241–255

    Google Scholar 

  • Buckley YM, Anderson S, Catterall CP, Corlett RT, Engel T, Gosper CR, Nathan R, Richardson DM, Setter M, Spiegel O, Vivian-Smith G, Voigt FA, Weir JES, Westcott DA (2006) Management of plant invasions mediated by frugivore interactions. J Appl Ecol 43:848–857

    Article  Google Scholar 

  • Cain ML, Milligan BG, Strand AE (2000) Long-distance seed dispersal in plant populations. Am J Bot 87:1217–1227

    Article  PubMed  CAS  Google Scholar 

  • Charalambidou I, Santamaria L, Langevoord O (2003) Effect of ingestion by five avian dispersers on the retention time, retrieval and germination of Ruppia maritima seeds. Funct Ecol 17:747–753

    Article  Google Scholar 

  • 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 

  • Cronk QCB, Fuller JL (1995) Plant invaders. Chapman & Hall, London

    Google Scholar 

  • Cull B, Lindsay P (1995) Fruit growing in warm climates: for commercial growers and home gardens. Reed Books, Chatswood

    Google Scholar 

  • Day MD, Wiley CJ, Playford J, Zalucki MP (2003) Lantana current management status and future prospects. ACIAR monograph 102

  • Debussche M, Isenmann P (1989) Fleshy fruit characters and the choices of bird and mammal seed dispersers in a Mediterranean region. Oikos 56:327–338

    Article  Google Scholar 

  • Evenari M (1949) Germination inhibitors. Bot Rev 15:153–194

    Article  Google Scholar 

  • Ferreras AE, Galetto L (2010) From seed production to seedling establishment: important steps in an invasive process. Acta Oecol 36:211–218

    Article  Google Scholar 

  • Firth DJ (1981) Camphor laurel (Cinnamomum camphora): a new weed in north-eastern New South Wales. Aust Weeds 1:26–28

    Google Scholar 

  • Fraser MW (1990) Foods of Redwinged Starlings and the potential for avian dispersal of Acacia cyclops at the Cape of Good Hope nature reserve. S Afr J Ecol 1:73–76

    Google Scholar 

  • Gosper CR, Vivian-Smith G (2009) The role of fruit traits of bird-dispersed plants in invasiveness and weed risk assessment. Divers Distrib 15:1037–1046

    Article  Google Scholar 

  • Gosper CR, Vivian-Smith G (2010) Fruit traits of vertebrate-dispersed alien plants: smaller seeds and more pulp sugar than indigenous species. Biol Invasions 12:2153–2163

    Article  Google Scholar 

  • Gosper CR, Stansbury CD, Vivian-Smith G (2005) Seed dispersal of fleshy-fruited invasive plants by birds: contributing factors and management options. Divers Distrib 11:549–558

    Article  Google Scholar 

  • Graaff JL (1987) The seed fly Ophiomyia lantanae and other factors responsible for reducing germination in Lantana camara forms found in Natal. S Afr J Bot 53:104–107

    Google Scholar 

  • Green RJ (1993) Avian seed dispersal in and near subtropical rain-forests. Wildl Res 20:535–557

    Article  Google Scholar 

  • Henderson L (2001) Alien weeds and invasive plants. Agricultural Research Council, Cape Town

    Google Scholar 

  • Higgins S, Richardson DM (1999) Predicting plant migration rates in a changing world: the role of long-distance dispersal. Am Nat 153:464–475

    Article  Google Scholar 

  • Hockey PAR, Dean WRJ, Ryan PG (2005) Roberts’ birds of Southern Africa. The trustees of the John Voelcker bird book fund, Cape Town

  • Howe HF (1986) Seed dispersal by fruit-eating birds and mammals. In: Murray D (ed) Seed dispersal. Academic Press, Sydney, pp 123–189

    Google Scholar 

  • Jordano P (1987) Patterns of mutualistic interactions in pollination and seed dispersal: connectance, dependence asymmetries, and coevolution. Am Nat 129:657–677

    Article  Google Scholar 

  • Jordano P (2000) Fruits and frugivory. In: Fenner M (ed) Seeds: the ecology of regeneration in plant communities. CABI Publishing, New York, pp 125–165

    Chapter  Google Scholar 

  • Kinnaird MF (1998) Evidence for effective seed dispersal by the Sulawesi Red-Knobbed Hornbill, Aceros cassidix. Biotropica 30:50–55

    Article  Google Scholar 

  • Lafleur NE, Rubega MA, Elphick CS (2007) Invasive fruits, novel foods, and choice: an investigation of European Starling and American Robin frugivory. Wilson J Ornithol 119:429–438

    Article  Google Scholar 

  • Li X-H (2004) Avian seed dispersal of the camphor tree (Cinnamomum camphora). Workshop on seed dispersal and frugivory in Asia, China. 6–9 Jan 2004, pp 12–13

  • Loyn RH, French K (1991) Birds and environmental weeds in south-eastern Australia. Plant Prot Q 6:137–149

    Google Scholar 

  • McKey D (1975) The ecology of coevolved seed dispersal systems. In: Gilbert LE, Raven P (eds) Coevolution of animals and plants. University of Texas Press, Austin, pp 159–191

    Google Scholar 

  • Meyer GA, Witmer MC (1998) Influence of seed processing by frugivorous birds on germination success of three North American shrubs. Am Midl Nat 140:129–139

    Article  Google Scholar 

  • Mitra SK, Bose TK (1985) Fruits of India: tropical and subtropical. Naya Prokash, Calcutta

    Google Scholar 

  • 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 

  • Moore PD (2001) The guts of seed dispersal. Nature 414:406–407

    Article  PubMed  CAS  Google Scholar 

  • Murray KG, Russell S, Picone CM, Winnettmurray K, Sherwood W, Kuhlmann ML (1994) Fruit laxatives and seed passage rates in frugivores: consequences for plant reproductive success. Ecology 75:989–994

    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 

  • Oatley TB (1984) Exploitation of a new niche by the Rameron Pigeon Columba arquatrix in Natal. In: Ledger J (ed) Proceedings of the fifth Pan-African ornithological congress. Southern African ornithological society, Lilongwe, 1980, pp 323–330

  • Olckers T (1999) Biological control of Solanum mauritianum Scopoli (Solanaceae) in South Africa: a review of candidate agents, progress and future prospects. Afr Entomol Memoir 1:65–73

    Google Scholar 

  • Olckers T, Zimmermann HG (1991) Biological control of silverleaf nightshade, Solanum elaeagnifolium, and bugweed, Solanum mauritianum, (Solanaceae) in South Africa. Agric Ecosyst Environ 37:137–155

    Article  Google Scholar 

  • Panetta FD (2001) Seedling emergence and seed longevity of the tree weeds Celtis sinensis and Cinnamomum camphora. Weed Res 41:83–95

    Article  Google Scholar 

  • Panetta FD, McKee J (1997) Recruitment of the invasive ornamental, Schinus terebinthifolius, is dependent upon frugivores. Aust J Ecol 22:432–438

    Article  Google Scholar 

  • Parsons WT, Cuthbertson EG (2001) Noxious weeds of Australia. CSIRO Publishing, Collingwood

    Google Scholar 

  • Rambuda TD, Johnson SD (2004) Breeding systems of invasive alien plants in South Africa: does Baker’s rule apply? Divers Distrib 10:409–416

    Article  Google Scholar 

  • Ray PK (2002) Breeding tropical and subtropical fruits. Alpha Science International Ltd., Pangbourne

    Google Scholar 

  • Renne IJ, Barrow WC, Randall LAJ, Bridges WC (2002) Generalized avian dispersal syndrome contributes to Chinese tallow tree (Sapium sebiferum, Euphorbiaceae) invasiveness. Divers Distrib 8:285–295

    Article  Google Scholar 

  • Richardson DM, van Wilgen BW (2004) Invasive alien plants in South Africa: how well do we understand the ecological impacts? S Afr J Sci 100:45–52

    Google Scholar 

  • Richardson DM, Allsopp N, D’Antonio CM, Milton SJ, Rejmanek M (2000a) Plant invasions—the role of mutualisms. Biol Rev 75:65–93

    Article  PubMed  CAS  Google Scholar 

  • Richardson DM, Pysek P, Rejmanek M, Barbour MG, Panetta FD, West CJ (2000b) Naturalization and invasion of alien plants: concepts and definitions. Divers Distrib 6:93–107

    Article  Google Scholar 

  • Ridley HN (1930) The dispersal of plants throughout the world. L. Reeve & Co, Kent

    Google Scholar 

  • Ross MA, Harper JL (1972) Occupation of biological space during seedling establishment. J Ecol 60:77–88

    Article  Google Scholar 

  • Sahu AK, Panda S (1998) Population dynamics of a few dominant plant species around industrial complexes, in West Bengal, India. Bombay Nat Hist Soc J 95:15–18

    Google Scholar 

  • Samson JA (1986) Tropical fruits. Longman Scientific & Technical, Essex

    Google Scholar 

  • Schupp EW (1993) Quantity, quality and the effectiveness of seed dispersal by animals. Vegetatio 108:15–29

    Google Scholar 

  • Sharma GR, Raghubanshi AS, Singh JS (2005) Lantana invasion: an overview. Weed Biol Manag 5:157–165

    Article  Google Scholar 

  • Sorensen AE (1984) Energy and passage time: experiments with fruit preference in European Blackbirds (Turdus merula). J Anim Ecol 53:545–557

    Article  Google Scholar 

  • Spies JJ (1983–1984) Hybridization potential of Lantana camara (Verbenaceae). Garcia De Orta Ser Bot 6:145–149

  • Stansbury CD, Vivian-Smith G (2003) Interactions between frugivorous birds and weeds in Queensland as determined from a survey of birders. Plant Prot Q 18:157–165

    Google Scholar 

  • Swarbrick JT, Willson BW, Hannan-Jones MA (1995) The biology of Australian weeds 25. Lantana camara L. Plant Prot Q 10:82–95

    Google Scholar 

  • Traveset A (1998) Effect of seed passage through vertebrate frugivores’ guts on germination: a review. Perspect Plant Ecol Evol Syst 1(2):151–190

    Article  Google Scholar 

  • Van Kleunen M, Johnson SD (2007) South African Iridaceae with rapid and profuse seedling emergence are more likely to become naturalized in other regions. J Ecol 95:674–681

    Article  Google Scholar 

  • van Wilgen BW, Richardson DM, Le Maitre DC, Marais C, Magadlela D (2001) The economic consequences of alien plant invasions: examples of impacts and approaches to sustainable management in South Africa. Environ Dev Sustain 3:145–168

    Article  Google Scholar 

  • van Wilgen BW, Reyers B, Le Maitre DC, Richardson DM, Schonegevel L (2008) A biome-scale assessment of the impact of invasive alien plants on ecosystem services in South Africa. J Environ Manag 89:336–349

    Article  Google Scholar 

  • Vivian-Smith G, Gosper CR, Wilson A, Hoad K (2006) Lantana camara and the fruit- and seed-damaging fly, Ophiomyia lantanae (Agromyzidae): seed predator, recruitment promoter or dispersal disrupter? Biol Control 36:247–257

    Article  Google Scholar 

  • Voigt FA, Farwig N, Johnson SD (2011) Interactions between the invasive tree Melia azedarach (Meliaceae) and native frugivores in South Africa. J Trop Ecol 27:355–363

    Article  Google Scholar 

  • Wheelwright NT (1985) Fruit-size, gape width, and the diets of fruit-eating birds. Ecology 66:808–818

    Article  Google Scholar 

  • Witkowski ETF, Garner RD (2008) Seed production, seed bank dynamics, resprouting and long-term response to clearing of the alien invasive Solanum mauritianum in a temperate to subtropical riparian ecosystem. S Afr J Bot 74:476–484

    Article  Google Scholar 

  • Witmer MC, Cheke AS (1991) The Dodo and the Tambalacoque tree: an obligate mutualism reconsidered. Oikos 61:133–137

    Article  Google Scholar 

  • Yagihashi T, Hayashida M, Miyamoto T (1998) Effects of bird ingestion on seed germination of Sorbus commixta. Oecologia 114:209–212

    Article  Google Scholar 

  • Yagihashi T, Hayashida M, Miyamoto T (1999) Effects of bird ingestion on seed germination of two Prunus species with different fruit-ripening seasons. Ecol Res 14:71–76

    Article  Google Scholar 

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Acknowledgments

Thank you to the National Research Foundation (NRF), the Gay Langmuir bursary fund, and Birdlife South Africa for funding this research. Ezemvelo KZN Wildlife provided permits for the birds used during this study and the UKZN Ethics Committee provided ethical clearance. Thank you to the many UKZN students, especially Justin Hart, Mark Brown, Amy-Leigh Wilson, Sandile Hadebe, and Precious N. Dlamini who assisted with data collection.

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  1. School of Biological and Conservation Sciences, University of KwaZulu-Natal, Private Bag X01, Scottsville, Pietermaritzburg, 3209, South Africa

    Lorinda A. Jordaan & Colleen T. Downs

  2. DST-NRF Centre for Invasion Biology, School of Biological and Conservation Sciences, University of KwaZulu-Natal, Private Bag X01, Scottsville, Pietermaritzburg, 3209, South Africa

    Steven D. Johnson

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  1. Lorinda A. Jordaan
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  2. Steven D. Johnson
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Correspondence to Colleen T. Downs.

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Jordaan, L.A., Johnson, S.D. & Downs, C.T. The role of avian frugivores in germination of seeds of fleshy-fruited invasive alien plants. Biol Invasions 13, 1917–1930 (2011). https://doi.org/10.1007/s10530-011-0013-z

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