Abstract
Native frugivores play an important role in native plant community dynamics by participating in seed dispersal. Today many island forests are invaded by introduced omnivores, such as rats, but their role in dispersing native plants is still little known. Here, we evaluated whether native seeds from New-Caledonian rainforests can germinate after passing through an invasive rat digestive tract and compared seed germinability and germination time between seeds ingested by invasive rats and native frugivores. We offered native fruits of Ficus racemigera and Freycinetia sulcata to the rats Rattus rattus and R. exulans, three flying foxes Pteropus spp. and the pigeon Ducula goliath. Our results showed that seeds can germinate after passing through an invasive rat digestive tract, and suggest that rats can disperse seeds of both plant species. However, invasive rats may be less efficient than native frugivores, as more seeds were destroyed when passing through rat digestive tracts than through native frugivores, and because germinability was lower and germination time was longer for seeds passing through invasive rats than through native frugivores. The reduced efficiency of rats may result from their generalized diet, the structure of their digestive tract, and/or their feeding behavior. In New-Caledonian rainforests, dispersal services on both plant species are likely well fulfilled by flying foxes and Ducula pigeons, but rats do not seem to be as efficient dispersers. Consequently, management measures to protect native frugivores should help to conserve seed dispersal services.
This is a preview of subscription content, access via your institution.



References
Aickin M, Gensler H (1996) Adjusting for multiple testing when reporting research results: the Bonferroni vs Holm methods. Am J Pub Health 86(5):726–728
Aslan CE, Zavaleta ES, Croll D, Tershy B (2012) Effects of native and non-native vertebrate mutualists on plants. Conserv Biol 26:778–789. doi:10.1111/j.1523-1739.2012.01885.x
Atkinson IAE (1985) The spread of commensal species of Rattus to oceanic islands and their effects on avifaunas. ICPB Tech Publ 3:35–81
Balouet JC (1991) The fossil vertebrate record of New Caledonia. In: Vickers-Rich P, Monaghan JM, Baird RF, Rich TH (eds) Vertebrate palaeontology of Australasia. Pioneer Design Studio/Monash University Publicartions Committee, Melbourne, pp 1383–1409
Balouet JC, Olson SL (1989) Fossil birds from late Quaternary deposits in New Caledonia. Smithsonian Institution Press, Washington
Banack SA (1998) Diet selection and resource use by flying foxes (genus Pteropus). Ecology 79:1949–1967
Barnea A, Yom-Tov Y, Friedman J (1991) Does ingestion by birds affect seed germination? Funct Ecol 5:394–402. doi:10.2307/2389811
Barré N, Dutson G (2000) Oiseaux de Nouvelle Calédonie. Liste commentée. Alauda 68(supplement):49p
Barré N, de GWichatitsky M, Lecoq R, Maillard J-C (2003) Contribution to the knowledge of the New Caledonian imperial pigeon Ducula goliath (Gray, 1859), with emphasis on sexual dimorphism. Notornis 50:155–160
Beauvais M-L, Coléno A, Jourdan H (eds) (2006) Invasive species in the New Caledonian archipelago. IRD, Paris
Blackburn TM, Cassey P, Duncan RP et al (2004) Avian extinction and mammalian introductions on oceanic islands. Science 305:1955–1958
Blanvillain C, Thorsen M (2003) The biology of the critically endangered Marquesan Imperial-Pigeon (Ducula galeata), Nuku Hiva, Marquesas Archipelago (French Polynesia). EMU 103:381–386. doi:10.1071/MU01022
Boissenin M, Brescia F (2014) Movements of the New Caledonian over-hunted flying foxes: implications for management. In: 16th Australasian bat society conference. Townsville, Australia
Boissenin M, Gomez S, Barré N et al (2006) Interactions entre l’avifaune frugivore et la flore ligneuse en forêt sèche de Nouvelle- Calédonie. IAC, Dry forest programme, Nouméa, New Caledonia
Bourgeois K, Suehs CM, Vidal E, Médail F (2005) Invasional meltdown potential: facilitation between introduced plants and mammals on French Mediterranean islands. Ecoscience 12:248–256
Bramley GN (2014) Home ranges and interactions of kiore (Rattus exulans) and Norway rats (R. norvegicus) on Kapiti Island, New Zealand. N Z J Ecol 38:328–334
Brescia F (2007) Amélioration des connaissances et recommandations pour la sauvegarde des populations de Mégachiroptères (roussettes) en Province Sud de la Nouvelle-Calédonie. Institut Agronomique néo-Calédonien
Burrows CJ (1996) Germination behaviour of seeds of the New Zealand woody species Coprosma foetidissima, Freycinetia baueriana, Hoheria angustifolia, and Myrsine australis. N Z J Bot 34:499–508. doi:10.1080/0028825X.1996.10410130
Calviño-Cancela M (2004) Ingestion and dispersal: direct and indirect effects of frugivores on seed viability and germination of Corema album (Empetraceae). Acta Oecol 26:55–64. doi:10.1016/j.actao.2004.03.006
Capizzi D, Bertolino S, Mortelliti A (2014) Rating the rat: global patterns and research priorities in impacts and management of rodent pests. Mammal Rev 44:148–162. doi:10.1111/mam.12019
Carpenter RJ, Read J, Jaffré T (2003) Reproductive traits of tropical rain-forest trees in New Caledonia. J Trop Ecol 19:351–365. doi:10.1017/S0266467403003407
Caut S, Angulo E, Courchamp F (2008) Dietary shift of an invasive predator: rats, seabirds and sea turtles. J Appl Ecol 45:428–437. doi:10.1111/j.1365-2664.2007.01438.x
Chimera CG, Drake DR (2010) Patterns of seed dispersal and dispersal failure in a hawaiian dry forest having only introduced birds: introduced birds, invasion, and dispersal failure. Biotropica 42:493–502. doi:10.1111/j.1744-7429.2009.00610.x
Clout MN, Tilley JAV (1992) Germination of miro (Prumnopitys ferruginea) seeds after consumption by New Zealand pigeons (Hemiphaga novaeseelandiae). N Z J Bot 30:25–28. doi:10.1080/0028825X.1992.10412882
Courchamp F, Chapuis J-L, Pascal M (2003) Mammal invaders on islands: impact, control and control impact. Biol Rev 78:347–383. doi:10.1017/S1464793102006061
De Carvalho-Ricardo MC, Uieda W, Fonseca RCB, Rossi MN (2014) Frugivory and the effects of ingestion by bats on the seed germination of three pioneering plants. Acta Oecol 55:51–57. doi:10.1016/j.actao.2013.11.008
Flannery TF (1995) Mammals of the South-West Pacific and Moluccan Islands. Cornell University Press, Ithaca, NY
Foster JT, Robinson SK (2007) Introduced birds and the fate of Hawaiian rainforests. Conserv Biol 21:1248–1257
Funakoshi K, Watanabe H, Kunisaki T (1993) Feeding ecology of the northern Ryukyu fruit bat, Pteropus dasymallus dasymallus, in a warm-temperate region. J Zool 230:221–230. doi:10.1111/j.1469-7998.1993.tb02684.x
Galindo-Gonzalez J, Guevara S, Sosa VJ (2000) Bat- and bird-generated seed rains at isolated trees in pastures in a tropical rainforest. Conserv Biol 14:1693–1703
Grant-Hoffman MN, Barboza PS (2010) Herbivory in invasive rats: criteria for food selection. Biol Invasions 12:805–825
Heer K, Albrecht L, Kalko EKV (2010) Effects of ingestion by neotropical bats on germination parameters of native free-standing and strangler figs (Ficus sp., Moraceae). Oecologia 163:425–435. doi:10.1007/s00442-010-1600-x
Jordaan LA, Johnson SD, Downs CT (2011) The role of avian frugivores in germination of seeds of fleshy-fruited invasive alien plants. Biol Invasions 13:1917–1930. doi:10.1007/s10530-011-0013-z
Jordano P (2014) Fruits and frugivory. In: Gallagher RS (ed) Seeds: the ecology of regeneration in plant communities, 3rd edn. CABI International, Oxfordshire, pp 10–61
Kaiser-Bunbury CN, Traveset A, Hansen DM (2010) Conservation and restoration of plant–animal mutualisms on oceanic islands. Perspect Plant Ecol Evol Syst 12:131–143
Kelly D, Robertson AW, Ladley JJ, et al (2006) Relative (un) importance of introduced animals as pollinators and dispersers of native plants. In: Biological invasions in New Zealand. Springer, 227–245
Lever C (1985) Naturalized mammals of the world. Longman, London
Lord JM (1991) Pollination and seed dispersal in Freycinetia baueriana, a dioecious liane that has lost its bat pollinator. N Z J Bot 29:83–86. doi:10.1080/0028825X.1991.10415545
Markl JS, Schleuning M, Forget PM et al (2012) Meta-Analysis of the Effects of Human Disturbance on Seed Dispersal by Animals: human Effects on Animal Seed Dispersal. Conserv Biol 26:1072–1081. doi:10.1111/j.1523-1739.2012.01927.x
McConkey KR, Drake DR (2006) Flying foxes cease to function as seed dispersers long before they become rare. Ecology 87:271–276
McConkey KR, O’Farrill G (2016) Loss of seed dispersal before the loss of seed dispersers. Biol Conserv 201:38–49. doi:10.1016/j.biocon.2016.06.024
McConkey KR, Meehan HJ, Drake DR (2005) Seed dispersal by Pacific pigeons (Ducula pacifica) in Tonga, western Polynesia. Emu 104:369–376
Meyer J-Y, Butaud J-F (2008) 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. doi:10.1007/s10530-008-9407-y
Mickelburgh S, Hutson AM, Racey PA (1992) Old World fruit bats: An action plan for their conservation. IUCN/SSC Chiroptera Specialist Group, Gland
Mittermeier RA, Turner WR, Larsen FW et al (2011) Global biodiversity conservation: the critical role of hotspots. In: Zachos FE, Habel JC (eds) Biodiversity Hotspots. Springer, Berlin Heidelberg, pp 3–22
Morat P, Jaffré T, Tronchet F et al (2012) Le référentiel taxonomique Florical et les caractéristiques de la flore vasculaire indigène de la Nouvelle-Calédonie. Adansonia 34:179–221. doi:10.5252/a2012n2a1
Nakamoto A, Kinjo K, Izawa M (2009) The role of Orii’s flying-fox (Pteropus dasymallus inopinatus) as a pollinator and a seed disperser on Okinawa-jima Island, the Ryukyu Archipelago, Japan. Ecol Res 24:405–414. doi:10.1007/s11284-008-0516-y
Nogales M, Nieves C, Illera JC et al (2005) Effect of native and alien vertebrate frugivores on seed viability and germination patterns of Rubia fruticosa (Rubiaceae) in the eastern Canary Islands. Funct Ecol 19:429–436
Olesen JM, Valido A (2004) Lizards and birds as generalized pollinators and seed dispersers of island plants. Ecol Insul Ecol Cabil Insul Palma Asoc Espanola Ecol Terr 229–249
Parsons JG, Cairns A, Johnson CN et al (2006) Dietary variation in spectacled flying foxes (Pteropus conspicillatus) of the Australian Wet Tropics. Aust J Zool 54:417–428. doi:10.1071/ZO06092
Pattemore DE, Wilcove DS (2011) Invasive rats and recent colonist birds partially compensate for the loss of endemic New Zealand pollinators. Proc R Soc B Biol Sci rspb20112036
Pérez-Méndez N, Jordano P, Valido A (2015) Downsized mutualisms: consequences of seed dispersers’ body-size reduction for early plant recruitment. Perspect Plant Ecol Evol Syst 17:151–159. doi:10.1016/j.ppees.2014.12.001
Perrin MR, Maddock AH (1983) Preliminary investigations of the digestive processes of the white-tailed rat Mystromys albicaudatus (Smith 1834). Afr J Zool 18:128–133
Reid S, Armesto JJ (2011) Avian gut-passage effects on seed germination of shrubland species in Mediterranean central Chile. Plant Ecol 212:1–10. doi:10.1007/s11258-010-9796-8
Richards GC (1990) The spectacled flying-fox, Pteropus conspicillatus (Chiroptera: Pteropodidae), in North Queensland. 2. Diet, seed dispersal and feeding ecology. Aust Mammal 13:25–31
Ringler D, Russell J, Jaeger A et al (2014) Invasive rat space use on tropical islands: implications for bait broadcast. Basic Appl Ecol 15:179–186. doi:10.1016/j.baae.2014.01.005
Sakaguchi EI, Itoh H, Uchida S, Horigome T (1987) Comparison of fibre digestion and digesta retention time between rabbits, guinea-pigs, rats and hamsters. Br J Nutr 58:149–158
Scheiner S, Willig M (2011) The theory of ecology. University of Chicago Press, Chicago
Shiels AB (2011) Frugivory by introduced black rats (Rattus rattus) promotes dispersal of invasive plant seeds. Biol Invasions 13:781–792
Shiels AB, Drake DR (2011) Are introduced rats (Rattus rattus) both seed predators and dispersers in Hawaii? Biol Invasions 13:883–894. doi:10.1007/s10530-010-9876-7
Shiels AB, Flores CA, Khamsing A et al (2012) Dietary niche differentiation among three species of invasive rodents (Rattus rattus, R. exulans, Mus musculus). Biol Invasions 15:1037–1048. doi:10.1007/s10530-012-0348-0
Shiels AB, Pitt WC, Sugihara RT, Witmer GW (2014) Biology and impacts of Pacific island invasive species. 11. Rattus rattus the Black Rat (Rodentia: Muridae). Pac Sci 68:145–184. doi:10.2984/68.2.1
Shilton LA, Altringham JD, Compton SG, Whittaker RJ (1999) Old World fruit bats can be long-distance seed dispersers through extended retention of viable seeds in the gut. Proc R Soc B Biol Sci 266:219–223. doi:10.1098/rspb.1999.0625
Staddon SC, Compton SG, Portch A (2010) Dispersal of fig seeds in the Cook Islands: introduced frugivores are no substitutes for natives. Biodivers Conserv 19:1905–1916. doi:10.1007/s10531-010-9811-3
Stone BC, Huynh K-L, Poppendieck H-H (1998) Pandanaceae. In: Kubitzki PDK (ed) Flowering Plants · Monocotyledons. Springer, Berlin Heidelberg, pp 397–404
Sugihara RT (1997) Abundance and diets of rats in two native Hawaiian forests. Pac Sci 51:189–198
Tassin J, Boissenin M, Barré N (2010) Can Ptilinopus greyii (Columbidae) disperse seeds in New Caledonia’s dry forests? Pac Sci 64:527–532. doi:10.2984/64.4.527
Traveset A (1998) Effect of seed passage through vertebrate frugivores’ guts on germination: a review. Perspect Plant Ecol Evol Syst 1:151–190
Traveset A, Richardson D (2006) Biological invasions as disruptors of plant reproductive mutualisms. Trends Ecol Evol 21:208–216. doi:10.1016/j.tree.2006.01.006
Traveset A, Rodríguez-Pérez J, Pías B (2008) Seed trait changes in dispersers’guts and consequences for germination and seedling growth. Ecology 89:95–106
Traveset A, Nogales M, Alcover JA et al (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. doi:10.1007/s10530-008-9395-y
Traveset A, Heleno R, Nogales M (2014) The ecology of seed dispersal. In: Gallagher RS (ed) Seeds: the ecology of regeneration in plant communities, 3rd edn. CABI International, Oxfordshire, pp 62–93
Tylianakis JM, Didham RK, Bascompte J, Wardle DA (2008) Global change and species interactions in terrestrial ecosystems. Ecol Lett 11:1351–1363. doi:10.1111/j.1461-0248.2008.01250.x
Van Der Pijl L (1957) The dispersal of plants by bats (chiropterochory). Acta Bot Neerlandica 6:291–315
Whittaker RJ, Fernandez-Palacios JM (2007) Island biogeography. Ecology, evolution, and conservation. Oxford University Press, New York
Williams PA, Karl BJ, Bannister P, Lee WG (2000) Small mammals as potential seed dispersers in New Zealand. Austral Ecol 25:523–532
Wood S (2006) Generalized Additive Models: An Introduction with R. CRC Press, Boca Raton
Wotton DM, Clout MN, Kelly D (2008) Seed retention times in the New Zealand pigeon (Hemiphaga novaezeelandiae novaeseelandiae). N Z J Ecol 32:1–6
Zavaleta ES, Hobbs RJ, Mooney HA (2001) Viewing invasive species removal in a whole-ecosystem context. Trends Ecol Evol 16:454–459
Acknowledgments
This study was funded by the Northern Province of New Caledonia to REFCOR project (Réponses des Ecosystèmes Forestiers au COntrôle des Rongeurs, Convention No 12C240). We are grateful to Mélanie Boissenin, Bruno Fogliani, Charly Zongo from IAC (Institut Agronomique Néo-Calédonien) and Philippe Marmey from IRD (Institut de Recherche pour le Développement) for the valuable discussions about the experiment. We thank Almudena Lorenzo, Oriane Lallemand and Marianne Bonzon from Michel Corbasson Zoological and Forest Park of Noumea, “Direction de l’Environnement” of the Southern Province of New Caledonia, who allowed us to work with imperial pigeons and flying foxes. We also thank Edouard Bourguet and Frédéric Rigault for their help in collecting fruits, Josepho Bahormal for his help in taking care of rats, and Carol Frost for English advice and useful comments on the paper draft.
Author information
Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Duron, Q., Garcia-Iriarte, O., Brescia, F. et al. Comparative effects of native frugivores and introduced rodents on seed germination in New-Caledonian rainforest plants. Biol Invasions 19, 351–363 (2017). https://doi.org/10.1007/s10530-016-1284-1
Received:
Accepted:
Published:
Issue Date:
Keywords
- Seed dispersal
- Seed destruction
- Rattus
- Flying foxes
- Frugivorous pigeon