Skip to main content
Log in

Do frugivorous birds concentrate their foraging activities on those alien plants with the most abundant and nutritious fruits in the South African Mediterranean-climate region?

  • Published:
Plant Ecology Aims and scope Submit manuscript

Abstract

Alien plants with abundant and nutritious fruits may compete more effectively for avian dispersal services than native shrubs. This premise was examined by comparing daily foraging activity (visitation frequency, foraging bird number and foraging period) by four frugivorous bird species of different size on fruits of two native and two alien shrub species co-occurring at four different sites. Also, the quantities of seeds consumed daily by each of the four birds species from fruits of the four shrub species were measured and compared with the numbers of fruits and seeds, and the mass of fruits present in the shrub canopies as well as with their fruit monosaccharide concentrations. The quantities of seed consumed daily by four different size bird species (Columba arquatrix, Colius striatus, Pycnonotus capensis, Zosterops pallidus subsp capensis) were positively correlated with the numbers of seeds per m2 of canopy area and with fruit mass and fruit monosaccharide content per m2 of canopy area, as well as with the monosaccharide concentration of individual fruits, except in the C. arquatrix (African olive pigeon). All four bird species displayed the highest daily visitation frequencies on fruits of the alien Solanum mauritianum which were more abundant and nutritious than fruits of the other alien Lantana camara and fruits the natives Olea europaea subsp africana and Chrysanthemoides monilifera. They also all consumed greater quantities of seed daily from fruits of the alien S. mauritianum than from fruits of the other shrub species. These results corroborate proposals that frugivorous birds concentrate their foraging activities on those alien plants with the most abundant and nutritious fruits.

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

Access this article

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Bennett ATD, Cuthill IC (1994) Ultraviolet vision in birds: What is its function? Vis Res 34:1471–1478

    Google Scholar 

  • Bibby CJ, Burgess ND, Hill DA, Mustoe S (2000) Bird census techniques. Academic Press, London

    Google Scholar 

  • Blendinger P, Loiselle B, Blake J (2008) Crop size, plant aggregation, and microhabitat type affect fruit removal by birds from individual melastome plants in the Upper Amazon. Oecologia 158:273–283

    Article  PubMed  Google Scholar 

  • Bradford DF, Smith CC (1977) Seed predation and seed number in Scheelea palm fruits. Ecology 58:667–673

    Article  Google Scholar 

  • Brown M, Downs C, Johnson S (2012) African red-winged starlings prefer hexose sugar solutions, but do not like them too sweet. J Ornithol 153:265–272

    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 

  • Burkhardt D (1982) Birds, berries and UV. Naturwissenschaften 69:153–157

    Article  PubMed  CAS  Google Scholar 

  • Buysse JAN, Merckx R (1993) An improved colorimetric method to quantify sugar content of plant tissue. J Exp Bot 44:1627–1629

    Article  CAS  Google Scholar 

  • Cowling RM, Richardson DM (1995) Fynbos: South Africa’s unique floral kingdom. Fernwood Press, Cape Town

    Google Scholar 

  • Deckers B, Verheyen K, Vanhellemont M, Maddens E, Muys B, Hermy M (2008) Impact of avian frugivores on dispersal and recruitment of the invasive Prunus serotina; in an agricultural landscape. Biol Invasions 10:717–727

    Article  Google Scholar 

  • Denslow SJ (1987) Fruit removal rates from aggregated and isolated bushes of the red elderberry, Sambucus pubens. Can J Bot 65:1229–1235

    Article  Google Scholar 

  • Downs CT, Brown M (2002) Nocturnal heterothermy and torpor in the Malachite Sunbird (Nectarinia famosa). Auk 119:251–260

    Google Scholar 

  • Drummond BA (2005) The selection of native and invasive plants by frugivorous birds in Maine. Northeast Nat 12:33–44

    Google Scholar 

  • Foster MS (1990) Factors influencing bird foraging preferences among conspecific fruit trees. Condor 92:844–854

    Article  Google Scholar 

  • Fuentes M (1994) Diets of fruit-eating birds: what are the causes of interspecific differences? Oecologia 97:134–142

    Google Scholar 

  • Germishuizen G, Meyer NL, Steenkamp Y, Kieth M (eds) (2006) A checklist of south African plants. South African Botanical Diversity Network report No. 41 SABONET, Pretoria

  • Gervais AJ, Noon BR, Willson MF (1999) Avian selection of the color-dimorphic fruits of salmonberry. Rubus spectabilis: a field experiment. Oikos 84:77–86

    Google Scholar 

  • Gosper CR (2004) Fruit characteristics of invasive bitou bush, Chrysanthemoides monilifera (Asteraceae), and a comparison with co-occurring native plant species. Aust J Bot 52:223–230

    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 

  • Greenberg C, Smith L, Levey D (2001) Fruit fate, seed germination and growth of an invasive vine–an experimental test of ‘sit and wait’ strategy. Biol Invasions 3:363–372

    Article  Google Scholar 

  • Henderson L (2011) Mapping of invasive alien plants: the contribution of the southern African Plant Invaders Atlas (SAPIA) to biological weed control. Afr Entomology 19:498–503

    Article  Google Scholar 

  • Herrera CM (1995) Plant-vertebrate seed dispersal systems in the Mediterranean: ecological, evolutionary, and historical determinants. Annu Rev Ecol Syst 26:705–727

    Google Scholar 

  • Herrera CM (2002) Seed dispersal by vertebrates. In: Herrera CM, Pellmyr O (eds) Plant–animal interactions: an evolutionary approach. Blackwell Science pp, New York, pp 20–185

    Google Scholar 

  • Herrera CM, Jordano P, Lopez-Soria L, Amat JA (1994) Recruitment of a mast-fruiting, bird-dispersed tree: bridging frugivore activity and seedling establishment. Ecol Monogr 64:315–344

    Article  Google Scholar 

  • Hockey PAR, Dean WRJ, Ryan, Ryan PG (eds) (2005) Roberts’ birds of Southern Africa, 7th edn. John Voelcker Bird Book Fund, Cape Town

    Google Scholar 

  • Howe HF (1993) Specialized and generalized dispersal systems: where does ‘The Paradigm’ Stand? Vegetatio 107(108):3–13

    Google Scholar 

  • Johnson RA, Willson MF, Thompson JN, Bertin RI (1985) Nutritional values of wild fruits and consumption by migrant frugivorous birds. Ecology 66:819–827

    Article  Google Scholar 

  • Jordaan LA, Johnson SD, Downs CT (2011) Digestion of fruit of invasive alien plants by three southern African avian frugivores. Ibis 153:863–867

    Article  Google Scholar 

  • Jordano P (2000) Fruits and frugivory. In: Fenner M (ed) Seeds: the ecology of regeneration in natural plant communities. CABI Publishers, Wallingford, pp 125–166

    Chapter  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 

  • Kelly D, Sork VL (2002) Mast seeding in perennial plants: why, how, where? Annu Rev Ecol Syst 33:427–447

    Article  Google Scholar 

  • Knight RS (1986) A comparative analysis of fleshy fruit displays in alien and native plants. In: Macdonald IAW, Kruger FJ, Ferrar AA (eds) The ecology and management of biological invasions in Southern Africa. Oxford University Press, Cape Town, pp 171–178

    Google Scholar 

  • Knight RS (1988) Aspects of plant dispersal in the south-western Cape with particular reference to the roles of birds as dispersal agents. University of Cape Town, South Africa, PhD dissertation

    Google Scholar 

  • Knight RS, Siegfried WR (1983) Inter-relationships between type, size and colour of fruits and dispersal in southern African trees. Oecologia 56:405–412

    Article  Google Scholar 

  • Kueffer C, Kronauer L, Edwards PJ (2009) Wider spectrum of fruit traits in invasive than native floras may increase the vulnerability of oceanic islands to plant invasions. Oikos 118:1327–1334

    Article  CAS  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

    Google Scholar 

  • Lambert F (1989) Fig-eating by birds in a Malaysian lowland rain forest. J Trop Ecol 5:401–412

    Article  Google Scholar 

  • Laska MS, Stiles EW (1994) Effects of fruit crop size on intensity of fruit removal in Viburnum prunifolium (Caprifoliaceae). Oikos 69:199–202

    Article  Google Scholar 

  • Lavergne C, Rameau J-C, Figier J (1999) The invasive woody weed Ligustrum robustum subsp. walkeri threatens native forests on La Reunion. Biol Invasions 1:377–392

    Article  Google Scholar 

  • Le Maitre DC, Midgley JJ (1992) Plant reproductive ecology. In: Cowling R (ed) The ecology of fynbos. Oxford University Press, Cape Town, pp135–174

  • Levey DJ, Martínez del Rio C (2001) It takes guts (and more) to eat fruit: lessons from avian nutritional ecology. The Auk 118:819–831

  • Malcarney HL, Martínez del Rio C, Apanius V (1994) Sucrose intolerance in birds: simpel nonlethal diagnostic methods and consequences for assimilation of complex carbohydrates. The Auk 111:170–177

    Article  Google Scholar 

  • Martínez del Rio C, Restrepo C (1993) Ecological and behavioral consequences of digestion in frugivorous animals. Plant Ecology 107/-108: 205–216

  • McNamara JM, Houston AI, Lima SL (1994) Foraging routines of small birds in winter: a theoretical investigation. J Avian Biol 25:287–302

    Article  Google Scholar 

  • McPherson JM (1988) Preferences of cedar waxwings in the laboratory for fruit species, colour and size: a comparison with field observations. Anim Behav 36(961–472):969

    Google Scholar 

  • Mokotjomela TM (2012) A comparison of bird foraging preferences for fruits of indigenous and alien shrubs and seed dispersal potentials in the Cape Floristic Region. PhD thesis Stellenbosch University, South Africa

  • Montaldo NH (2000) Reproductive success of bird-dispersed plants in a subtropical forest relict in Argentina. Revista Chilena de Historia Natur 73:511–524

    Google Scholar 

  • Mucina L, Rutherford MC (eds) (2006) The vegetation of South Africa, Lesotho and Swaziland. Strelitzia 19, South African National Biodiversity Institute, Pretoria

  • Ortiz-Pulido R, Albores-Barajas YV, Diaz SA (2007) Fruit removal efficiency and success: influence of crop size in a neotropical treelet. Plant Ecol 189:147–154

    Article  Google Scholar 

  • Pysek P, Richardson DM (2007) Traits associated with invasiveness in alien plants: where do we stand? In: Nentwig W (ed) Biological invasions, vol 193., Ecological studies. Springer, Berlin, pp 97–125

  • Richardson DM, van Wilgen BW (2004) Invasive alien plants in South Africa: how well do we understand the ecological impacts? S Afr J Sci 100:42–52

    Google Scholar 

  • Richardson DM, Macdonald IAW, Holmes PM, Cowling RM (1992) Plant and animal invasions. In: Cowling RM (ed) The ecology of fynbos: nutrients, fire and diversity Oxford University Press, Cape Town, pp 271–308

  • Robertson AW, Trass A, Ladley JJ, Kelly D (2006) Assessing the benefits of frugivory for seed germination: the importance of the de-inhibition effect. Funct Ecol 20:58–66

    Article  Google Scholar 

  • Rowan MK (1983) The doves, parrots, louries, and cuckoos of southern Africa. John Voelcker bird book fund, Claremont

    Google Scholar 

  • Sakai AK, Allendorf FW, Holt JS, Lodge DM, Molofsky J, With KA, Baughman S, Cabin RJ, Cohen JE, Ellstrand NC, McCauley DE, O’Neil P, Parker IM, Thompson JN, Weller SG (2001) The population biology of invasive species. Annu Rev Ecol Syst 32:305–332

    Article  Google Scholar 

  • Sallabanks R (1993) Hierarchical mechanisms of fruit selection by an avian frugivore. Ecology 74:1326–1336

    Article  Google Scholar 

  • Sallabanks R, Courtney SP (1993) On fruit-frugivore relationships: variety is the spice of life. Oikos 68:567–570

    Article  Google Scholar 

  • Saracco JF, Jaime AC, Martha JG, Tomás AC (2005) Crop size and fruit neighborhood effects on bird visitation to fruiting Schefflera morototoni trees in Puerto Rico. Biotropica 37:81–87

    Article  Google Scholar 

  • Sargent S (1990) Neighborhood effects on fruit removal by birds: a field experiment with Viburnum Dentatum (Caprifoliaceae). Ecology 71:1289–1298

    Article  Google Scholar 

  • Schaefer HM, Schmidt V, Bairlein F (2003) Discrimination abilities for nutrients: which difference matters for choosy birds and why? Anim Behav 65:531–541

    Article  Google Scholar 

  • Schupp EW (1993) Quantity, quality and the effectiveness of seed dispersal by animals. Vegetatio 107(108):15–29

    Google Scholar 

  • Schupp EW, Jordano P, Gómez JM (2010) Seed dispersal effectiveness revisited: a conceptual review. New Phytol 188:333–353

    Article  PubMed  Google Scholar 

  • Schurr FM, Spiegel O, Steinitz O, Trakhtenbrot A, Tsoar A, Nathan N (2009) Long-distance seed dispersal. Annual Plant Reviews 38:204–237

    Google Scholar 

  • Scott JK (1996) Population ecology of Chrysanthemiodes monilifera in South Africa: implications for its control in Australia. J Appl Ecol 33:1496–1508

    Article  Google Scholar 

  • Siitari H, Honkavaara J, Viitala J (1999) Ultraviolet reflection of berries attracts foraging birds. A laboratory study with redwings (Turdus iliacus) and bilberries (Vaccinium myrtillus). Proc Royal Soc London 26:2125–2129

    Google Scholar 

  • Spiegel O, Nathan R (2007) Incorporating dispersal distance into the disperser effectiveness framework: frugivorous birds provide complementary dispersal to plants in a patchy environment. Ecol Lett 10:718–728

    Article  PubMed  Google Scholar 

  • Steadman DW (1997) The historic biogeography and community ecology of Polynesian pigeons and doves. J Biogeogr 24:737–753

    Article  Google Scholar 

  • Tsoar A, Shohami D, Nathan R (2011) A movement ecology approach to study seed dispersal and plant invasion: an overview and application of seed dispersal by fruit bats. Fifty years of invasion ecology. In: Richardson DM (ed) The legacy of Charles Elton. Wiley-Blackwell, Oxford, pp 103–119

    Google Scholar 

  • Underhill LG, Hofmeyr JH (2007) Barn Swallows Hirundo rustica disperse seeds of rooikrans Acacia cyclops, an invasive alien plant in the Fynbos Biome. Ibis 149:468–471

    Article  Google Scholar 

  • Valido A, Schaefer HM, Jordano P (2011) Colour, design and reward: phenotypic integration of fleshy fruit displays. J Evol Biol 24:751–760

    Article  PubMed  CAS  Google Scholar 

  • van Wyk B, van Wyk P (1997) Field guide to trees of southern Africa. Struik Publishers, Cape Town

    Google Scholar 

  • Vazquez DP, Morris WF, Jordano P (2005) Interaction frequency as a surrogate for the total effect of animal mutualists on plants. Ecol Lett 8:1088–1094

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Willson MF, Whelan CJ (1989) Ultraviolet reflectance of fruits of vertebrate-dispersed plants. Oikos 55:341–348

    Article  Google Scholar 

  • Witmer MC (1998) Ecological and evolutionary implications of energy and protein requirements of avian frugivores eating sugary diets. Physiol Zool 71:599–610

    PubMed  CAS  Google Scholar 

  • Witmer MC, Soest PJV (1998) Contrasting digestive strategies of fruit-eating birds. Funct Ecol 12:728–741

    Article  Google Scholar 

Download references

Acknowledgments

Funds for this project were provided by the Andrew Mellon Foundation, the Oppenheimer Memorial Trust and Lesotho Government which were administered by the South African National Biodiversity Institute and the University of Stellenbosch who also provided research facilities. Mr. Stanley Snyders provided technical assistance in the field. Mrs Judith Arnolds provided guidance in fruit nutritional essays and Mr. Leslie Powrie in extraction of plant distribution records from SANBI databases.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Thabiso Michael Mokotjomela.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mokotjomela, T.M., Musil, C.F. & Esler, K.J. Do frugivorous birds concentrate their foraging activities on those alien plants with the most abundant and nutritious fruits in the South African Mediterranean-climate region?. Plant Ecol 214, 49–59 (2013). https://doi.org/10.1007/s11258-012-0145-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11258-012-0145-y

Keywords

Navigation