Hostname: page-component-586b7cd67f-t8hqh Total loading time: 0 Render date: 2024-11-23T18:51:48.316Z Has data issue: false hasContentIssue false
  • English
  • Français

Tree recruitment after native frugivore extinction? A field experiment to test the impact of fruit flesh persistence in a tropical oceanic island

Published online by Cambridge University Press:  24 June 2022

Sébastien Albert Open the ORCID record for Sébastien Albert [Opens in a new window] ,
Olivier Flores Open the ORCID record for Olivier Flores [Opens in a new window] ,
Mikael Stahl ,
Florian Guilhabert  and
Dominique Strasberg
Sébastien Albert*
Affiliation:
Université de la Réunion, UMR PVBMT, Saint-Denis, La Réunion 97400, France
Olivier Flores
Affiliation:
Université de la Réunion, UMR PVBMT, Saint-Denis, La Réunion 97400, France
Mikael Stahl
Affiliation:
Université de la Réunion, UMR PVBMT, Saint-Denis, La Réunion 97400, France
Florian Guilhabert
Affiliation:
Université de la Réunion, UMR PVBMT, Saint-Denis, La Réunion 97400, France
Dominique Strasberg
Affiliation:
Université de la Réunion, UMR PVBMT, Saint-Denis, La Réunion 97400, France OSU-Réunion, Université de la Réunion, Saint-Denis, La Réunion 97400, France
*
Author for correspondence: Sébastien Albert, Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The loss of large frugivores leads to seed dispersal loss and regeneration failure of numerous large-seeded trees near mother trees. Although Janzen–Connell effects are considered as the primary underlying cause, other factors remain understudied. Here, we used a field experiment to test the impact of flesh persistence on the recruitment of two large-seeded Sapotaceae species that lost their dispersers. In the rainforest of Mare Longue (Réunion), we sowed 3840 seeds in a four-factor design: seed treatment (seed cleaning; flesh persistence), canopy closure (understory; gap), year of sowing (01/2018; 11/2019) and species (Labourdonnaisia calophylloides, Mimusops balata). We also used camera traps to evaluate the impact of extant vertebrates. Seed treatment was by far the most influential factor: flesh persistence led to seedling recruitment divided by 3,2 on average, mainly due to failure of germination or seedling emergence. There were also significant variations in recruitment between species, years and canopy closure levels, notably due to the behaviour of the invasive fauna, especially giant snails that could unexpectedly restore recruitment by feeding on fruit flesh. Together, our results demonstrate strongly depleted recruitment due to flesh persistence and the importance of field experiments to understand the processes at work in complex ecosystems with novel plant–animal interactions.

Keywords

Biological invasiondormancyfrugivore extinctionisland biologyJanzen–Connell hypothesisSapotaceaeseed predation
Type
Research Article
Information
Journal of Tropical Ecology , Volume 38 , Issue 6 , November 2022 , pp. 370 - 376
Check for updates
Copyright
© The Author(s), 2022. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Albert, S (2020) Rupture des interactions mutualistes plantes à fruits charnus-vertébrés frugivores, et conséquences sur la régénération des forêts tropicales dans les Mascareignes . Doctoral dissertation. Université de La Réunion.Google Scholar
Albert, S, Flores, O, Baider, C, Florens, FBV and Strasberg, D (2021) Differing severity of frugivore loss contrasts the fate of native forests on the land of the Dodo (Mascarene archipelago). Biological Conservation 257, 109131.CrossRefGoogle Scholar
Albert, S, Flores, O, Michon, L and Strasberg, D (2020a) Dating young (<1000 yr) lava flow eruptions of Piton de la Fournaise volcano from size distribution of long-lived pioneer trees. Journal of Volcanology and Geothermal Research 401, 106974.CrossRefGoogle Scholar
Albert, S, Flores, O and Strasberg, D (2020b) Collapse of dispersal trait diversity across a long-term chronosequence reveals a strong negative impact of frugivore extinctions on forest resilience. Journal of Ecology 108, 1386–1397.CrossRefGoogle Scholar
Baider, C and Florens, FBV (2006) Current decline of the ‘Dodo-tree’: a case of broken-down interactions with extinct species or the result of new interactions with alien invaders. In Laurance W and Peres CA (eds.), Emerging Threats to Tropical Forests, Chicago: Chicago University Press, pp. 199–214.Google Scholar
Baider, C and Florens, FBV (2011) Control of invasive alien weeds averts imminent plant extinction. Biological Invasions 13, 2641–2646.CrossRefGoogle Scholar
Barnea, A, Yom-Tov, Y and Friedman, J (1991) Does ingestion by birds affect seed ermination? Functional Ecology 5, 394.CrossRefGoogle Scholar
Baskin, JM and Baskin, CC (2004) A classification system for seed dormancy. Seed Science Research 14, 1–16.CrossRefGoogle Scholar
Bissessur, P, Baider, C and Florens, FBV (2020) Infestation by pollination-disrupting alien ants varies temporally and spatially and is worsened by alien plant invasion. Biological Invasions 22, 2573–2585.CrossRefGoogle Scholar
Cadet, T (1977) La végétation de l’île de la Réunion: étude phytoécologique et phytosociologique (Doctoral dissertation), Université d’Aix-Marseille.Google Scholar
Cheke, AS (1987) The ecology of the surviving native land-birds of Reunion. In Diamond, AW (ed.), Studies of Mascarene Island Birds. Cambridge: Cambridge University Press, pp. 301–358.CrossRefGoogle Scholar
Comita, LS, Queenborough, SA, Murphy, SJ, … Zhu, Y (2014) Testing predictions of the Janzen-Connell hypothesis: a meta-analysis of experimental evidence for distance- and density-dependent seed and seedling survival. Journal of Ecology 102, 845–856.CrossRefGoogle ScholarPubMed
Connell, JH (1971) On the role of natural enemies in preventing competitive exclusion in some marine animals and in rain forest trees. In Den Boer PJ and Gradwell GR (eds), Dynamics of Populations, 298, 298–312.Google Scholar
Debroize, N (2003) Le grand natte (Mimusops maxima) en forêt mégatherme hygrophile à l'île de la Réunion. Montpellier: ENGREF, 76 p. Mémoire: Ecole nationale du génie rural, des eaux et des forêts.Google Scholar
Effiom, EO, Nunez-Iturri, G, Smith, HG, Ottosson, U and Olsson, O (2013) Bushmeat hunting changes regeneration of African rainforests. Proceedings of the Royal Society B: Biological Sciences 280, 20130246.CrossRefGoogle ScholarPubMed
Eriksson, O, Friis, EM and Löfgren, P (2000) Seed size, fruit size, and dispersal systems in angiosperms from the early Cretaceous to the late Tertiary. The American Naturalist 156, 47–58.CrossRefGoogle Scholar
Fedriani, JM, Zywiec, M and Delibes, M (2012) Thieves or mutualists? Pulp feeders enhance endozoochore local recruitment. Ecology 93, 575–587.CrossRefGoogle ScholarPubMed
Hansen, DM, Kaiser, CN and Müller, CB (2008) Seed dispersal and establishment of endangered plants on oceanic islands: the Janzen-Connell model, and the use of ecological analogues. PLoS ONE 3, e2111.CrossRefGoogle ScholarPubMed
Harrison, RD, Tan, S, Plotkin, JB … Davies, SJ (2013) Consequences of defaunation for a tropical tree community. Ecology Letters 16, 687–694.CrossRefGoogle ScholarPubMed
Hopkins, M and Graham, AW (2006) The viability of seeds of rainforest species after experimental soil burials under tropical wet lowland forest in north-eastern Australia. Australian Journal of Ecology 12, 97–108.CrossRefGoogle Scholar
Janzen, DH (1970) Herbivores and the number of tree species in tropical forests. American Naturalist 104, 501–528.CrossRefGoogle Scholar
Levi, T and Peres, CA (2013) Dispersal vacuum in the seedling recruitment of a primate-dispersed Amazonian tree. Biological Conservation 163, 99–106.CrossRefGoogle Scholar
Loayza, AP, Luna, CA and Calviño-Cancela, M (2020) Predators and dispersers: context-dependent outcomes of the interactions between rodents and a megafaunal fruit plant. Scientific Reports 10, 6106.CrossRefGoogle Scholar
Macdonald, IAW, Thébaud, C, Strahm, WA and Strasberg, D (1991) Effects of alien plant invasions on native vegetation remnants on La Réunion (Mascarene Islands, Indian Ocean). Environmental Conservation 18, 51–61.CrossRefGoogle Scholar
Mahandran, V, Murugan, CM, Marimuthu, G and Nathan, PT (2018) Seed dispersal of a tropical deciduous Mahua tree, Madhuca latifolia (Sapotaceae) exhibiting bat-fruit syndrome by pteropodid bats. Global Ecology and Conservation 14, e00396.CrossRefGoogle Scholar
Mandon-Dalger, I, Clergeau, P, Tassin, J, Rivière, J-N and Gatti, S (2004) Relationships between alien plants and an alien bird species on Reunion Island. Journal of Tropical Ecology 20, 635–642.CrossRefGoogle Scholar
Meunier, JD, Kirman, S, Strasberg, D, Nicolini, E, Delcher, E and Keller, C (2010) The output and bio-cycling of Si in a tropical rain forest developed on young basalt flows (La Reunion Island). Geoderma 159, 431–439.CrossRefGoogle Scholar
Meyer, WM and Shiels, AB (2009) Black rat (Rattus rattus) predation on nonindigenous snails in Hawai‘i: complex management implications. Pacific Science 63, 339–347.CrossRefGoogle Scholar
Porter, RH, Durrel, M and Romm, HJ (1947) The use of 2, 3, 5-triphenyl-tetrazolium chloride as a measure of seed germinability. Plant Physiology 22, 149–159.CrossRefGoogle Scholar
Réchou, A, Flores, O, Jumeaux, G … Bonnardot, F (2019) Spatio-temporal variability of rainfall in a high tropical island: patterns and large-scale drivers in Réunion Island. Quarterly Journal of the Royal Meteorological Society 145, 893–909.CrossRefGoogle Scholar
Rick, CM and Bowman, RI (1961) Galapagos tomatoes and tortoises. Evolution 15, 407–417.CrossRefGoogle Scholar
Rogers, HS, Cavazos, BR, Gawel, AM, Karnish, A, Ray, CA, Rose, E, Thierry, H and Fricke, EC (2021 PREPRINT). Frugivore gut passage increases seed germination: an updated meta-analysis. Preprint at http://biorxiv.org/lookup/doi/10.1101/2021.10.12.462022.CrossRefGoogle Scholar
Shiels, AB and Drake, DR (2011) Are introduced rats (Rattus rattus) both seed predators and dispersers in Hawaii? Biological Invasions 13, 883–894.CrossRefGoogle Scholar
Silvius, KM and Fragoso, JMV (2002) Pulp handling by vertebrate seed dispersers increases palm seed predation by Bruchid beetles in the northern Amazon. Journal of Ecology 90, 1024–1032.CrossRefGoogle Scholar
Soltani, E, Baskin, CC, Baskin, JM, Heshmati, S and Mirfazeli, MS (2018) A meta-analysis of the effects of frugivory (endozoochory) on seed germination: role of seed size and kind of dormancy. Plant Ecology 219, 1283–1294.CrossRefGoogle Scholar
Strasberg, D (1996) Diversity, size composition and spatial aggregation among trees on a 1-ha rain forest plot at La Réunion. Biodiversity & Conservation 5, 825–840.CrossRefGoogle Scholar
Temple, SA (1977) Plant-animal mutualism: coevolution with dodo leads to near extinction of plant. Science 197, 885–886.CrossRefGoogle ScholarPubMed
Terborgh, J (2012) Enemies maintain hyperdiverse tropical forests. The American Naturalist 179, 303–314.CrossRefGoogle ScholarPubMed
Terborgh, J, Nuñez-Iturri, G, Pitman, NCA … Paine, CET (2008) Tree recruitment in an empty forest. Ecology 89, 1757–1768.CrossRefGoogle Scholar
Tillier, S (1992) Introduced land snails in New Caledonia: a limited impact in the past, a potential disaster in the future. Pacific Science 46, 396–397.Google Scholar
Traveset, A (1998) Effect of seed passage through vertebrate frugivores’ guts on germination: a review. Perspectives in Plant Ecology, Evolution and Systematics 1, 151–190.CrossRefGoogle Scholar
Trolliet, F, Bauman, D, Forget, P-M, Doucet, J-L, Gillet, J-F and Hambuckers, A (2019) How complementary are large frugivores for tree seedling recruitment? A case study in the Congo Basin. Journal of Tropical Ecology 35, 223–236.CrossRefGoogle Scholar
van der Pijl, L (1982) Principles of Dispersal in Higher Plants, Third Revised and Expanded Edition. Berlin Heidelberg, New York: Springer Verlag.CrossRefGoogle Scholar
Vanthomme, H, Bellé, B and Forget, P-M (2010) Bushmeat hunting alters recruitment of large-seeded plant species in Central Africa. Biotropica 42, 672–679.CrossRefGoogle Scholar
Vazquez-Yanes, C and Orozco-Segovia, A (1993) Patterns of seed longevity and germination in the tropical rainforest. Annual Review of Ecology and Systematics 24, 69–87.CrossRefGoogle Scholar
Vizentin-Bugoni, J, Tarwater, CE, Foster, JT … Sperry, JH (2019) Structure, spatial dynamics, and stability of novel seed dispersal mutualistic networks in Hawai‘i. Science 364, 78–82.CrossRefGoogle ScholarPubMed
Wyse Jackson, PS, Cronk, QCB and Parnell, JAN (1988) Notes on the regeneration of two rare Mauritian endemic trees. Tropical Ecology 29, 98–106.Google Scholar
Supplementary material: File

Albert et al. supplementary material

Albert et al. supplementary material 1

Download Albert et al. supplementary material(File)
File 71.3 KB
Supplementary material: File

Albert et al. supplementary material

Albert et al. supplementary material 2

Download Albert et al. supplementary material(File)
File 25.4 MB