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Mistletoe specialist frugivores: latterday ‘Johnny Appleseeds’ or self-serving market gardeners?

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Abstract

Many plants use birds to disperse their propagules, but mistletoes are especially reliant on their services. As aerial parasites, mistletoe seeds need to be deposited upon branches of suitable hosts, and mistletoe specialist frugivores (from eight different avian families) have long been regarded as their coevolved dispersers. Like the pioneer Johnny ‘Appleseed’ Chapman who established nurseries that helped open up land for settlement, these birds are considered benevolent dispersers of this keystone resource and often invoked as illustrative examples of mutualistic interactions. We have compared recent research on these specialists with studies of other birds with broader diets (generalists) which also disperse mistletoe seed. Rather than mutualists, we suggest that mistletoe specialist frugivores are better considered exploitative, with multiple lineages evolving independently to capitalize on this reliable, nutritious resource. Although mistletoe specialist frugivores are quantitatively important seed dispersers in some regions, their specialized diet restricts them to areas with high mistletoe densities, resulting in contagious dispersal patterns. By intensifying existing infections, mistletoe specialist frugivores increase their own medium-term food security—akin to market gardeners profiting from intensive cultivation. Exploring the ecological and evolutionary implications of this proposition, we evaluate the consequences of different dispersal patterns on mistletoe fitness and highlight the neglected role of dietary generalists in the stabilization of plant–animal interactions.

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References

  • Amico G, Aizen MA (2000) Mistletoe seed dispersal by a marsupial. Nature 408:929–930

    PubMed  CAS  Google Scholar 

  • Aukema JE (2003) Vectors, viscin, and Viscaceae: mistletoes as parasites, mutualists, and resources. Front Ecol Environ 1:212–219

    Article  Google Scholar 

  • Aukema JE, Martínez del Rio C (2002) Variation in mistletoe seed deposition: effects of intra- and interspecific host characteristics. Ecography 25:139–144

    Article  Google Scholar 

  • Aukema JE, Martìnez del Rio C (2002) Mistletoes as parasites and seed-dispersing birds as disease vectors: current understanding challenges and opportunities. In: Levey DJ, Silva WR, Galetti M (eds) Seed dispersal and frugivory: ecology, evolution and conservation. CAB International, Wallingford, pp 99–110

    Google Scholar 

  • Barea LP (2008) Interactions between frugivores and their resources: case studies with the Painted Honeyeater Grantiella picta. PhD thesis. Charles Sturt University, Albury

  • Barea LP, Watson DM (2007) Temporal variation in food resources determines onset of breeding in an Australian mistletoe specialist. Emu 107:203–209

    Article  Google Scholar 

  • Bascompte J, Jordano P (2007) The structure of plant–animal mutualistic networks: the architecture of biodiversity. Annu Rev Ecol Evol Syst 38:567–593

    Article  Google Scholar 

  • Bowie M, Ward D (2004) Water and nutrient status of the mistletoe Plicosepalus acaciae parasitic on isolated Negev Desert populations of Acacia raddiana differing in level of mortality. J Arid Environ 56:487–508

    Article  Google Scholar 

  • Carlo TA, Aukema JE (2005) Female-directed dispersal and facilitation between a tropical mistletoe and a dioecious host. Ecology 86:3245–3251

    Article  Google Scholar 

  • Carlo TA, Collazo JA, Groom MJ (2003) Avian fruit preferences across a Puerto Rican forested landscape: pattern consistency and implications for seed removal. Oecologia 134:119–131

    Article  PubMed  Google Scholar 

  • Frick WF, Price RD, Heady PA, Kay KM (2013) Insectivorous bat pollinates columnar cactus more effectively per visit than specialized nectar bat. Am Nat 181:137–144

    Article  PubMed  Google Scholar 

  • Godschalk SKB (1983) Mistletoe dispersal by birds in South Africa. In: Calder M, Bernhardt P (eds) The biology of mistletoes. Academic Press, Sydney, pp 117–128

    Google Scholar 

  • Green AK, Ward D, Griffiths ME (2009) Directed dispersal of mistletoe (Plicosepalus acaciae) by yellow-vented bulbuls (Pycnonotus xanthopygos). J Ornith 150:167–173

    Article  Google Scholar 

  • Herrera CM (1985) Determinants of plant–animal coevolution: the case of mutualistic dispersal of seeds by vertebrates. Oikos 44:132–141

    Article  Google Scholar 

  • Howe HF, Estabrook GF (1977) On intraspecific competition for avian dispersers in tropical trees. Am Nat 111:817–832

    Article  Google Scholar 

  • Ingwell LL, Eigenbrode SD, Bosque-Peŕez NA (2012) Plant viruses alter insect behavior to enhance their spread. Sci Rep 2:578. doi:10.1038/srep00578

    Article  PubMed  Google Scholar 

  • Jordano P, García C, Godoy JA, García-Castaño JL (2007) Differential contribution of frugivores to complex seed dispersal patterns. Proc Natl Acad Sci USA 104:3278–3282

    Article  PubMed  CAS  Google Scholar 

  • Kuijt J (1964) Critical observations on the parasitism of New World mistletoes. Can J Bot 42:1243–1287

    Article  Google Scholar 

  • Larson D (1996) Seed dispersal by specialist versus generalist foragers: the plant’s perspective. Oikos 76:113–120

    Article  Google Scholar 

  • Lewis EE, Campbell JF, Sukhdeo MVK (2002) The behavioural ecology of parasites. CAB International, Wallingford

    Book  Google Scholar 

  • Mack AL, Wright DD (1998) The vulturine parrot (Psittrichas fulgidus), a threatened New Guinea endemic: notes on its biology and conservation. Bird Conserv Int 8:185–194

    Article  Google Scholar 

  • Martínez del Rio C, Medel RSA, Hourdequin M (1996) Seed dispersers as disease vectors: bird transmission of mistletoe seeds to plant hosts. Ecology 77:912–921

    Article  Google Scholar 

  • Montaño-Centellas FA (2013) Effectiveness of mistletoe seed dispersal by tyrant flycatchers in a mixed Andean landscape. Biotropica 45:209–216

    Article  Google Scholar 

  • Murphy SR, Reid N, Yan ZG, Venables WN (1993) Differential passage time of mistletoe fruits through the gut of honeyeaters and flowerpeckers—effects on seedling establishment. Oecologia 93:171–176

    Article  Google Scholar 

  • Rawsthorne J, Watson DM, Roshier DA (2011) Implications of movement patterns of a dietary generalist for mistletoe seed dispersal. Austral Ecol 36:650–655

    Google Scholar 

  • Rawsthorne J, Watson DM, Roshier DA (2012) The restricted seed rain of a mistletoe specialist. J Avian Biol 43:9–14

    Article  Google Scholar 

  • Reid N (1986) Pollination and seed dispersal of mistletoes (Loranthaceae) by birds in southern Australia. In: Ford HA, Paton DC (eds) The dynamic partnership: birds and plants in southern Australia. SA Government Printer, Adeleide, pp 64–84

    Google Scholar 

  • Reid N (1989) Dispersal of mistletoes by honeyeaters and flowerpeckers—components of seed dispersal quality. Ecology 70:137–145

    Article  Google Scholar 

  • Reid N (1991) Coevolution of mistletoes and frugivorous birds. Aust J Ecol 16:457–469

    Article  Google Scholar 

  • Reid N, Yan Z, Fittler J (1994) Impact of mistletoes (Amyema miquelii) on host (Eucalyptus blakelyi and Eucalyptus melliodora) survival and growth in temperate Australia. For Ecol Manag 70:55–65

    Article  Google Scholar 

  • Restrepo C (1987) Aspectos ecológicos de la diseminación de cinco especies de muérdagos por aves. Humboldtia 1:65–116

    Google Scholar 

  • Restrepo C, Sargent S, Levey DJ, Watson DM (2002) The role of vertebrates in the diversification of new world mistletoes. In: Levey DJ, Silva WR, Galetti M (eds) Seed dispersal and frugivory: ecology, evolution and conservation. CAB International, Wallingford, pp 83–98

    Google Scholar 

  • Richardson KC, Wooller RD (1988) The alimentary-tract of a specialist frugivore, the mistletoebird, Dicaeum hirundinaceum, in relation to its diet. Aust J Zool 36:373–382

    Article  Google Scholar 

  • Rödl T, Ward D (2002) Host recognition in a desert mistletoe: early stages of development are influenced by substrate and host origin. Funct Ecol 16:128–134

    Article  Google Scholar 

  • Sargent S (1994) Seed dispersal of mistletoes by birds in Monteverde, Costa Rica. PhD thesis. Cornell University, Ithaca

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

    Google Scholar 

  • Shaw DC, Watson DM, Mathiasen RL (2004) Comparison of dwarf mistletoes (Arceuthobium spp., Viscaceae) in the western United States with mistletoes (Amyema spp., Loranthaceae) in Australia—ecological analogs and reciprocal models for ecosystem management. Aust J Bot 52:481–498

    Article  Google Scholar 

  • Snow DW (1981) Tropical frugivorous birds and their food plants: a world survey. Biotropica 13:1–14

    Article  Google Scholar 

  • Snow B, Snow D (1988) Birds and berries. Poyser, Calton

  • Soto-Gamboa M, Bozinovic F (2002) Fruit-disperser interaction in a mistletoe-bird system: a comparison of two mechanisms of fruits processing on seed germination. Plant Ecol 159:171–174

    Article  Google Scholar 

  • Thomson J (2003) When is it mutualism? Am Nat 162[Suppl]:S1–S9

    Article  PubMed  Google Scholar 

  • van Ommeren RJ, Whitham TG (2002) Changes in interactions between juniper and mistletoe mediated by shared avian frugivores: parasitism to potential mutualism. Oecologia 130:281–288

    Google Scholar 

  • Walsberg GE (1975) Digestive adaptations of Phainopepla nitens associated with the eating of mistletoe berries. Condor 77:169–174

    Article  Google Scholar 

  • Walsberg GE (1977) Ecology and energetics of contrasting social systems in Phainopepla nitens (Aves: Ptilogonatidae). University of California Press, Berkeley

    Google Scholar 

  • Ward MJ, Paton DC (2007) Predicting mistletoe seed shadow and patterns of seed rain from movements of the mistletoebird Dicaeum hirundinaceum. Austral Ecol 32:113–121

    Article  Google Scholar 

  • Watson DM (2001) Mistletoe—a keystone resource in forests and woodlands worldwide. Annu Rev Ecol Syst 32:219–249

    Article  Google Scholar 

  • Watson DM (2004) Mistletoe—a unique constituent of canopies worldwide. In: Lowman M, Rinker B (eds) Forest canopies. Elsevier, San Diego, London, pp 212–223

    Chapter  Google Scholar 

  • Watson DM (2009) Determinants of parasitic plant distribution: the role of host quality. Botany 87:16–21

    Article  Google Scholar 

  • Watson DM (2011) Mistletoes of southern Australia. CSIRO Publishing, Collingwood

    Google Scholar 

  • Watson DM (2013) The relative contribution of specialists and generalists to mistletoe dispersal: insights from a neotropical rain forest. Biotropica 45:195–202

    Article  Google Scholar 

  • Watson DM, Herring M (2012) Mistletoe as a keystone resource: an experimental test. Proc R Soc B 279:3853–3860

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We are grateful to Tomás Carlo and Patrick Kavanagh for their insightful comments on an earlier version of this manuscript, and we thank Laurence Barea and Karolina Petrovic for their contributions to initial discussions. DMW received support from the Australian Research Council (DP0449417) and Charles Sturt University.

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Correspondence to David M. Watson.

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Communicated by Carlos L. Ballare.

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Watson, D.M., Rawsthorne, J. Mistletoe specialist frugivores: latterday ‘Johnny Appleseeds’ or self-serving market gardeners?. Oecologia 172, 925–932 (2013). https://doi.org/10.1007/s00442-013-2693-9

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  • DOI: https://doi.org/10.1007/s00442-013-2693-9

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