Abstract
Seed dispersal is crucial for the success and spread of alien plants. Herbivores often establish a dual relationship with plants: antagonist, through herbivory, and mutualist, through seed dispersal. By consuming plants, herbivores may disperse large amounts of seeds, and can facilitate the spread of alien plants. However, seed dispersal of alien plants by herbivores has been largely uninvestigated. I studied factors associated with dispersal of alien and native seeds by the three most important vertebrate herbivores in SW Australia: emus (Dromaius novaehollandia), western grey kangaroos (Macropus fuliginosus) and European rabbits (Oryctolagus cuniculus). Overall frequencies of alien and native seeds dispersed by these herbivores were determined by differences among them in (1) the plant groups they predominantly disperse, that differed in frequencies of aliens versus natives, and (2) the predominant dispersal of aliens or natives within those plant groups. Emus and kangaroos (natives) tended to disperse predominantly alien seeds within plant groups (defined by life forms, dispersal syndromes, and diaspore size), whereas rabbits (alien) tended to disperse predominantly natives. This agrees with the hypothesis that herbivores will use predominantly plants that have evolved in different areas, because of less effective defences against new enemies. Overall frequencies were consistent with this pattern in kangaroos and rabbits, but not in emus. Kangaroos dispersed mostly plant groups that were mainly aliens (herbaceous species and small and medium sized dispersal units and seeds), which together with their predominant use of aliens over natives within groups resulted in the highest overall frequency of alien seeds (73%). Rabbits were similar to kangaroos in the type of plants dispersed, but their predominant use of natives over aliens within groups contributed to an overall predominance of native seeds in their pellets (88%). Emus dispersed mostly plant groups that were mainly natives (e.g. woody species with big diaspores), resulting in low overall frequency of alien seeds (11%), despite their predominant use of aliens over natives within plant groups. Thus, the within-groups trend pointed to a facilitative role of native herbivores of plant invasions through seed dispersal, but was obscured by the different use by herbivores of plant groups with different frequency of aliens.
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References
Abdi H, Valentin D (2007) Multiple correspondence analysis. In: Salkind N (ed), Encyclopedia of measurement and statistics, Sage
Benvenuti S (2007) Weed seed movement and dispersal strategies in the agricultural environment. Weed Biol Manag 7:141–157
Benzécri JP (1979) Sur le calcul des taux d’inertie dans l’analyse d’un questionnaire. Cahiers de l’Analyse des Données 4:377–378
Bernays EA, Chapman RF (1994) Host-plant selection by phytophagous insects. Chapman and Hall
Calviño-Cancela M, Dunn RR, van Etten E, Lamont BB (2006) Emus as non-standard seed dispersers and their potential for long-distance dispersal. Ecography 29:632–640
Calviño-Cancela M, Ayres Fernández C, Cordero Rivera A (2007) European pond turtles (Emys orbicularis) as alternative dispersers of “water-dispersed” waterlily (Nymphaea alba): effects on viability and germination. Écoscience 14:529–534
Calviño-Cancela M, He TH, Lamont BB (2008) Distribution of myrmecochorous species over the landscape and their potential long-distance dispersal by emus and kangaroos. Divers Distrib 14:11–17
Clifford HT, Drake WE (1985) Seed dispersal by kangaroos and their relatives. J Trop Ecol 1:373–374
Cosyns E, Hoffmann M (2005) Horse dung germinable seed content in relation to plant species abundance, diet composition and seed characteristics. Basic Appl Ecol 6:11–24
Cosyns E, Delporte A, Lens L, Hoffmann M (2005) Germination success of temperate grassland species after passage through ungulate and rabbit guts. J Ecol 93:353–361
Davies SJJF (2002) Ratites and tinamous. Bird families of the world, Oxford University Press
Davis NE, Coulson G, Forsyth DM (2008) Diets of native and introduced mammalian herbivores in shrub-encroached grassy woodland, south-eastern Australia. Wildlife Res 35:684–694
Dawson TJ, Read D, Russel EM, Herd RM (1984) Seasonal variation in daily activity patterns, water relations and diet of Emus. Emu 84:93–102
Dellow DW (1982) Studies on the nutrition of macropodine marsupials III. The flow of digesta through the stomach and intestine of macropodines and sheep. Aust J Zool 30:751–765
Dodd J, Martin RJ, Howes KM (1993) Management of agricultural weeds in Western Australia. Dep.of Agric, WA
Flematti GR, Ghisalberti EL, Dixon KW, Trengove RD (2004) A compound from smoke that promotes seed germination. Science 305:977
Forbes DK, Tribe DE (1970) The utilisation of roughages by sheep and kangaroos. Aust J Zool 18:247–256
Fukunaga K (1990) Statistical pattern recognition. Academic press
Gunn B (2001) Australian Tree Seed Centre Operations Manual. CSIRO
Herd RM, Dawson TJ (1984) Fibre digestion in the emu, Dromaius novaehollandie, a large bird with a simple gut and high rates of passage. Phys Zool 57:70–84
Higgins SI, Nathan R, Cain ML (2003) Are long-dispersal distance events in plants usually caused by non-standard means of dispersal? Ecology 84:1945–1956
Hopper S, Gioia P (2004) The southwest Australia floristic region: evolution and conservation of a global spot of biodiversity. Annu Rev Ecol Evol S 35:623–650
Janzen D (1984) Dispersal of small seeds by big herbivores: foliage is the fruit. Am Nat 123:338–353
Jordano P (2000) Fruits and frugivory. In: Fenner M (ed) Seeds: the ecology of regeneration in plant communities. CAB International, Wallingford, pp 125–165
Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170
King DR, Wheeler SH, Oliver AJ (1985) The European rabbit flea, Spilopsyllus cuniculi, in southwestern Australia. Aust Wildlife Res 12:227–236
Levine JM, Adler PB, Yelenik SG (2004) A meta-analysis of biotic resistance to exotic plant invasions. Ecol Letters 7:975–989
Malo JE, Suárez F (1995) Herbivorous mammals as seed dispersers in a Mediterranean dehesa. Oecologia 104:246–255
Malo JE, Jiménez B, Suárez F (1995) Seed bank build-up in small disturbances in a Mediterranean pasture: the contribution of endozoochorous dispersal by rabbits. Ecography 18:73–82
Maron JL, Vilà M (2001) When do herbivores affect plant invasion? Evidence for the natural enemies and biotic resistance hypotheses. Oikos 95:361–373
Martin GR, Twigg LE, Zampichelli L (2007) Seasonal changes in the diet of the European rabbit (Oryctolagus cuniculus) from three different Mediterranean habitats in south-western Australia. Wildlife Res 34:25–42
Moles AT, Ackerly DD, Webb CO et al (2005) Factors that shape seed mass evolution. Proc Natl Acad Sci USA 102:10540–10544
Moseby KE, De Jong S, Munro N, Pieck A (2005) Home range, activity and habitat use of European rabbits (Oryctolagus cuniculus) in arid Australia: implications for control. Wildlife Res 32:305–311
Myers N et al (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858
Pakeman RJ, Engelen J, Attwood JP (1999) Rabbit endozoochory and seedbank build up in an acidic grassland. Plant Ecol 145:83–90
Pakeman RJ, Digneffe G, Small JL (2002) Ecological correlates of endozoochory by herbivores. Funct Ecol 16:296–304
Parker JD, Burkepile DE, Hay ME (2006) Opposing effects of native and exotic herbivores on plant invasions. Science 311:1459–1461
Richardson DM, Allsopp N, D’Antonio CM, Milton SJ, Rejmanek M (2000) Plant invasions—the role of mutualisms. Biol Rev 75:65–93
Simberloff D, Von Holle B (1999) Positive interactions of nonindigenous species: invasional meltdown? Biol Invasions 1:21–32
Sokal RR, Rohlf FJ (1995). Biometry. Freeman and Co
StatSoft, Inc. (2007) STATISTICA (data analysis software system), version 8.0. www.statsoft.com
Stiles EW (2000) Animals as seed dispersers. In: Fenner M (ed) Seeds: the ecology of regeneration in plant communities. CAB International, Wallingford, pp 111–124
Stott P (2003) Use of space by sympatric European hares (Lepus europaeus) and European rabbits (Oryctolagus cuniculus) in Australia. Mammal Biol 68:317–327
Viggers KL, Hearn JP (2005) The kangaroo conundrum: home range studies and implications for land management. J Appl Ecol 42:99–107
Wann JM, Bell DT (1997) Dietary preferences of the black-gloved wallaby (Macropus irma) and the western grey kangaroo (M. fuliginosus) in Whiteman Park, Perth, WA. J R Soc WA 80:55–62
Williams K, Parer I, Coman B, Burley J, Braysher M (1995) Managing vertebrate pests: rabbits. Bureau of Resource Sciences, Australia
Acknowledgments
I thank Byron Lamont for plant and seed identification and kind support during my stage in Curtin University (Perth, Australia), Ken Okamitsu for processing some of the samples, Peter Mioduszewski for assistance in the greenhouse, the Spanish Ministry of Education and Science for a postdoctoral fellowship in Australia and the Department of Environment and Conservation for permission to work in reserves. Plant identifications were confirmed with reference collections at the Western Australian Herbarium, Perth. During the preparation of the manuscript I was supported by a Isidro Parga Pondal contract (Xunta de Galicia). I thank Marc Cadotte and anonymous referees for their comments on previous versions of the manuscript.
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Calvino-Cancela, M. Seed dispersal of alien and native plants by vertebrate herbivores. Biol Invasions 13, 895–904 (2011). https://doi.org/10.1007/s10530-010-9877-6
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DOI: https://doi.org/10.1007/s10530-010-9877-6