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Seed dispersal by proboscis monkeys: the case of Nauclea spp.

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Abstract

Frugivorous vertebrates such as primates are important dispersal agents in tropical forests, although the role of folivorous colobines is generally not considered. However, recent studies reported seed dispersal by endo- and epizoochory in colobine primates, including the proboscis monkey (Nasalis larvatus), suggesting that the role colobines play in seed dispersal might have been underestimated. In the Lower Kinabatangan Floodplain in Sabah, Malaysian Borneo, we investigated whether seeds were still able to germinate after being ingested by proboscis monkeys. Faecal samples (n = 201) from proboscis monkeys were collected between 2015 and 2017. Intact seeds belonging to eight plant species were found in 77% of the faecal samples. Nauclea spp. were the most abundant plant species, accounting for 98% of all intact seeds. This study is the first to conduct germination trials on seeds defecated by proboscis monkeys. Higher germination success was recorded in ingested Nauclea spp. seeds than in control seeds, from both ripe and unripe Nauclea orientalis fruits (P < 0.001). Therefore, we suggest that proboscis monkeys play a role in seed dispersal by enhancing the germination success of defecated seeds for at least some plant species. Similar to other colobines, although proboscis monkeys may provide a lower contribution to seed dispersal (low seed diversity over short distances) than other sympatric frugivores, this study emphasises that proboscis monkeys do contribute to the dispersal of intact seeds, such as Nauclea spp., in potentially suitable riverine habitats.

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References

  • Abram NK, Xofis P, Tzanopoulos J, Macmillan DC, Ancrenaz M, Chung R, Peter L, Ong R, Lackman I, Goossens B, Ambu L, Knight AT (2014) Synergies for improving oil palm production and forest conservation in floodplain landscapes. PLoS One 9:e95388. https://doi.org/10.1371/journal.pone.0095388

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Albert A, Hambuckers A, Culot L, Savini T, Huynen MC (2013) Frugivory and seed dispersal by Northern pigtailed macaques (Macaca leonina), in Thailand. Int J Primatol 34:170–193

    Article  Google Scholar 

  • Andresen E, Levey DJ (2004) Effects of dung and seed size on secondary dispersal, seed predation, and seedling establishment of rain forest trees. Oecologia 139:45–54

    Article  PubMed  Google Scholar 

  • Arditti J, Michaud JD, Allison PO (1981) Seed germination of North American orchids. I. Native California and related species of Calypso, Epipactis, Goodyera, Piperia, and Platanthera. Bot Gaz 142:442–453

    Article  Google Scholar 

  • Arthur JC (1985) Deviation in development due to the use of unripe seeds. Am Nat 29:804–815

    Article  Google Scholar 

  • Azmi R (1998) Natural vegetation of the Kinabatangan Floodplain. Part 1: an introduction to its natural vegetation, including a preliminary plant checklist of the region. WWF-Malaysia, Kota Kinabalu

  • Barnea A, Yom-Tov Y, Friedman J (1990) Differential germination of two closely related species of Solanum in response to bird ingestion. Oikos 57:222–228

    Article  Google Scholar 

  • Barnea A, Yom-Tov Y, Friedman J (1992) Effect of frugivorous birds on seed dispersal and germination of multi-seeded fruits. Acta Oecol 13:209–219

    Google Scholar 

  • Barnett AA, Boyle SA, Pinto LP, Lourenc WC, Almeida T, Silva WS, Ronchi-Teles B, Bezerra BM, Ross C, MacLarnon A, Spironello WR (2012) Primary seed dispersal by three Neotropical seed-predating primates (Cacajao melanocephalus ouakary, Chiropotes chiropotes and Chiropotes albinasus). J Trop Ecol 28:543–555

    Article  Google Scholar 

  • Boland DJ, Brooker MIH, Chippendale GM, Hall N, Hyland BPM, Johnston RD, Kleinig DA, McDonald MW, Turner JD (2006) Forest trees of Australia, 5th edn. CSIRO Publishing, Collingwood

    Book  Google Scholar 

  • Chapman CA (1995) Primate seed dispersal: coevolution and conservation implications. Evol Anthropol 4:74–82

    Article  Google Scholar 

  • Chen Y, Chen H, Zhang Y, Yao H, Yang W, Zhao Y, Ruan X, Xiang Z (2018) First evidence of epizoochorous seed dispersal by golden snub-nosed monkeys (Rhinopithecus roxellana) in temperate forest. Plant Ecol 219:417–427

    Article  Google Scholar 

  • Corlett RT (2017) Frugivory and seed dispersal by vertebrates in tropical and subtropical Asia: an update. Glob Ecol Conserv 11:1–22

    Article  Google Scholar 

  • Corlett RT, Lucas PW (1990) Alternative seed-handling strategies in primates: seed-spitting by long-tailed macaques (Macaca fascicularis). Oecologia 82:166–171

    Article  CAS  PubMed  Google Scholar 

  • Cruz-Tejada DM, Acosta-Rojas DC, Stevenson PR (2018) Are seeds able to germinate before fruit color ripening? Evidence from six Neotropical bird-dispersed plant species. Ecosphere 9:e02174. https://doi.org/10.1002/ecs2.2174

    Article  Google Scholar 

  • Dasilva GL (1994) Diet of Colobus polykomos on Tiwai Island: selection of food in relation to its seasonal abundance and nutritional quality. Int J Primatol 15:655–680

    Article  Google Scholar 

  • Davies AG, Bennett EL, Waterman PG (1988) Food selection by two South-east Asian colobine monkeys (Presbytis rubicunda and Presbytis melalophos) in relation to plant chemistry. Biol J Linn Soc 34:33–56

    Article  Google Scholar 

  • Ehlers Smith DA, Husson SJ, Ehlers Smith YC, Harrison ME (2013) Feeding ecology of red langurs in Sabangau tropical peat-swamp forest, Indonesian Borneo: extreme granivory in a non-masting forest. Am J Primatol 9999:1–12

    Google Scholar 

  • Evenari M (1949) Germination inhibitors. Bot Rev 15:153–194

    Article  Google Scholar 

  • Farwig N, Berens DG (2012) Imagine a world without seed dispersers: a review of threats, consequences and future directions. Basic Appl Ecol 13:109–115

    Article  Google Scholar 

  • Foster MS (1977) Ecological and nutritional effects of food scarcity on a tropical frugivorous bird and its fruit source. Ecology 58:73–85

    Article  CAS  Google Scholar 

  • Garber PA, Lambert JE (1998) Primates as seed dispersers: ecological processes and directions for future research. Am J Primatol 45:3–8

    Article  CAS  PubMed  Google Scholar 

  • Hanya G, Bernard H (2012) Fallback foods of red leaf monkeys (Presbytis rubicunda) in Danum Valley, Borneo. Int J Primatol 33:322–337

    Article  Google Scholar 

  • Hodgkison R, Balding ST, Zubaid A, Kunz TH (2003) Fruit bats (Chiroptera: Pteropodidae) as seed dispersers and pollinators in a lowland Malaysian rain forest. Biotropica 35:491–502

    Article  Google Scholar 

  • Howe HE, Smallwood J (1982) Ecology of seed dispersal. Annu Rev Ecol Syst 13:201–228

    Article  Google Scholar 

  • Kassambara A, Kosinski M, Biecek P, Fabian S (2017) Package ‘survminer’: drawing survival curves using ‘ggplot2’. R package version 0.4.1. https://CRAN.R-project.org/package=survminer

  • Lim TK (2013) Edible medicinal and non-medicinal plants: fruits, vol 5. Springer, New York

    Book  Google Scholar 

  • Loiselle BA (1990) Seeds in droppings of tropical fruit-eating birds: importance of considering seed composition. Oecologia 82:494–500

    Article  PubMed  Google Scholar 

  • Matsuda I, Tuuga A, Higashi S (2009) The feeding ecology and activity budget of proboscis monkeys. Am J Primatol 71:478–492

    Article  PubMed  Google Scholar 

  • Matsuda I, Tuuga A, Bernard H (2011) Riverine refuging by proboscis monkeys (Nasalis larvatus) and sympatric primates: implications for adaptive benefits of the riverine habitat. Mamm Biol 76:165–171

    Article  Google Scholar 

  • Matsuda I, Higashi S, Otani Y, Tuuga A, Bernard H, Corlett RT (2013) A short note on seed dispersal by colobines: the case of the proboscis monkey. Integr Zool 8:395–399

    Article  PubMed  Google Scholar 

  • Matsuda I, Sha JCM, Ortmann S, Schwarm A, Grandl F, Caton J, Jens W, Kreuzer M, Marlena D, Hagen KB, Clauss M (2015) Excretion patterns of solute and different-sized particle passage markers in foregut-fermenting proboscis monkey (Nasalis larvatus) do not indicate an adaptation for rumination. Physiol Behav 149:45–52

    Article  CAS  PubMed  Google Scholar 

  • McConkey KR (2018) Seed dispersal by primates in Asian habitats: from species, to communities, to conservation. Int J Primatol 39:466–492

    Article  Google Scholar 

  • McNair JN, Sunkara A, Frobish D (2012) How to analyse seed germination data using statistical time-to-event analysis: non-parametric and semi-parametric methods. Seed Sci Res 22:77–95

    Article  Google Scholar 

  • Meijaard E, Nijman V, Supriatna J (2008) Nasalis larvatus. The IUCN red list of threatened species 2008: e.T14352A4434312. https://doi.org/10.2305/IUCN.UK.2008.RLTS.T14352A4434312.en. Downloaded on 23 July 2019

  • Meyer GA, Witmet MC (1998) Influence of seed processing by frugivorous birds on germination success of three North American shrubs. Am Midl Nat 140:129–139

    Article  Google Scholar 

  • Nguyen H, Bai B, Li N, Pan Y, Lu (2013) Fruit diet, selectivity and seed dispersal of Hatinh langur (Tachypithecus francoisi hatinhensis). Acta Ecol Sin 33:110–119

    Article  Google Scholar 

  • Nijboer J (2006) Fibre intake and faeces quality in leaf-eating primates. Dissertation, Universiteit Utrecht

  • Nijboer J, Clauss M (2006) The digestive physiology of colobine primates. In: Nijboer J (ed) Fibre intake and faeces quality in leaf-eating primates. Universiteit Utrecht, Utrecht, pp 9–28

    Google Scholar 

  • Norconk MA, Grafton BW, Conklin-Brittain NL (1998) Seed dispersal by neotropical seed predators. Am J Primatol 45:103–126

    Article  CAS  PubMed  Google Scholar 

  • Pettit NE, Froend RH (2001) Availability of seed for recruitment of riparian vegetation: a comparison of a tropical and a temperate river ecosystem in Australia. Aust J Bot 49:515–528

    Article  Google Scholar 

  • Ranglack G, Yeager C (1986) Survey of intestinal parasites found in proboscis monkeys (Nasalis larvatus) and long-tailed macaques (Macaca fascicularis). Primate Rep 14:249

    Google Scholar 

  • Razafindratsima OH, Sato H, Tsuji Y, Culot L (2018) Advances and frontiers in primate seed dispersal. Int J Primatol 39:315–320

    Article  Google Scholar 

  • R Development Core Team (2017) R: a language and environment for statistical computing. R foundation for statistical computing. R 3.4.3. Vienna

  • Samuels IA, Levey DJ (2005) Effects of gut passage on seed germination: do experiments answer the questions they ask? Funct Ecol 19:365–368

    Article  Google Scholar 

  • Serio-Silva J, Rico-Gray V (2003) Howler monkeys (Alouatta palliata mexicana) as seed dispersers of strangler figs in disturbed and preserved habitat in Southern Veracruz, Mexico. In: Marsh LK (ed) Primates in fragments: ecology and conservation. Springer, Boston, pp 267–281

    Chapter  Google Scholar 

  • Shepherd VE, Chapman CA (1998) Dung beetles as secondary seed dispersers: impact on seed predation and germination. J Trop Ecol 14:199–215

    Article  Google Scholar 

  • Stark DJ (2018) Habitat use and movement of proboscis monkeys (Nasalis larvatus) in a degraded and human-modified forest landscape. PhD Thesis, Cardiff University

  • Stark DJ, Vaughan IP, Saldivar DAR, Nathan SKSS, Goossens B (2017) Evaluating methods for estimating home ranges using GPS collars: a comparison using proboscis monkeys (Nasalis larvatus). PLoS One 12:1–23. https://doi.org/10.1371/journal.pone.0174891

    Article  CAS  Google Scholar 

  • Terborgh J, Pitman N, Silman M, Schichter H, Núñez VP (2002) Maintenance of tree diversity in tropical forests. In: Levey DJ, Silva WR, Galetti M (eds) Seed dispersal and frugivory: ecology, evolution and conservation. CAB International, Wallingford, pp 1–17

    Google Scholar 

  • Therneau TM (2015) A package for survival analysis in S. version 2.38. https://CRAN.R-project.org/package=survival

  • Traveset A, Bermejo T, Willson M (2001) Effect of manure composition on seedling emergence and growth of two common shrub species of Southeast Alaska. Plant Ecol 155:29–34

    Article  Google Scholar 

  • Traveset A, Robertson AW, Rodríguez-Pérez J (2007) A review on the role of endozoochory in seed germination. In: Dennis AJ, Schupp EW, Green RJ, Westcott DA (eds) Seed dispersal: theory and its application in a changing world. CAB International, Wallingford, pp 78–103

    Chapter  Google Scholar 

  • Trolliet F, Serckx A, Forget P, Beudels-Jamar RC, Huynen MC, Hambuckers A (2016) Ecosystem services provided by a large endangered primate in a forest-savanna mosaic landscape. Biol Conserv 203:55–66

    Article  Google Scholar 

  • Tsuji Y, Ningsih JIDP, Kitamura S, Widayati KA, Suryobroto B (2017) Neglected seed dispersers: endozoochory by Javan lutungs (Trachypithecus auratus) in Indonesia. Biotropica 49:539–545

    Article  Google Scholar 

  • Waterman PG, Kool KM (1994) Colobine food selection and plant chemistry. In: Davies AG, Oates JF (eds) Colobine monkeys: their ecology, behaviour, and evolution. Cambridge University Press, Cambridge, pp 251–284

    Google Scholar 

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Acknowledgements

We are grateful to the Sabah Biodiversity Centre and the Sabah Wildlife Department for supporting our research project and allowing us to conduct this study in the Lower Kinabatangan Wildlife Sanctuary. This project would not have been possible without financial support from the FNRS (Fonds de la Recherche Scientifique), the FNRS Gustave Boël-Sofina Fellowship and the Fonds Léopold III—pour l’Exploration et la Conservation de la Nature asbl. We thank Quentin Phillipps for his invaluable contribution, as well as all the students and research assistants at Danau Girang Field Centre who worked with us in the field. Finally, we thank the two anonymous reviewers for their valuable comments that improved the manuscript.

Funding

This study was funded by FNRS (2014-18100, 2016-16755), FNRS Gustave Boël-Sofina Fellowship (2016) and Fonds Léopold III—pour l’Exploration et la Conservation de la Nature asbl. (2014-14.118).

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Correspondence to Valentine Thiry.

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No direct contact with animals was conducted during this research, and ethical aspects of the research protocols have been approved by the FNRS committee and Sabah Biodiversity Council.

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Thiry, V., Bhasin, O., Stark, D.J. et al. Seed dispersal by proboscis monkeys: the case of Nauclea spp.. Primates 60, 449–457 (2019). https://doi.org/10.1007/s10329-019-00736-x

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