Functional guild complementarity and morphological filtering in Annonaceae seed dispersal within a managed tropical garden

Main Article Content

TRI HANDAYANI
HARY WAWANGNINGRUM
MUHAMMAD EFENDI
YUZAMMI
TITUT YULISTYARINI

Abstract

Abstract. Handayani T, Wawangningrum H, Yuzammi, Efendi M, Yulistyarini T. 2026. Functional guild complementarity and morphological filtering in Annonaceae seed dispersal within a managed tropical garden. Nusantara Bioscience 18 (1): n180103. https://doi.org/10.13057/nusbiosci/n180103. Understanding the mechanisms that structure plant-frugivore interactions in managed ex situ environments is essential for maintaining Seed Dispersal Effectiveness (SDE), genetic diversity, and long-term plant persistence. This study assessed the possible morphological filtering effect of Annonaceae fruit and seed traits on four co-existing frugivore guilds (birds, bats, squirrels, and civets) in the protected environment of the Bogor Botanical Gardens (BBG), Indonesia. To ensure a comprehensive dataset, we performed detailed morphological measurements and conducted twice-weekly observations across 22 Annonaceae species to identify fruit consumption patterns. We recorded fruit color, size, and shape, and statistically tested the classical morphological filtering hypothesis using Chi-Square, ANOVA, and Spearman correlation analyses. Our results showed a generally generalist interaction system, with the apocarpous fruit type being the most prevalent (12 species). The morphological specialization hypothesis was rejected, as fruit and seed size dimensions did not significantly correlate with specific visitor guilds (χ² = 9.793, df = 18, P = 0.938). Spearman’s rank correlation confirmed strong internal morphological constraints within the fruit (ρ > 0.70, P < 0.05), while no external ecological filtering regarding animal attraction was detected (ρ > 0.70, P > 0.05). This pattern indicates that frugivores in these managed collections exhibit high behavioral flexibility, utilizing a broad range of resources regardless of specific morphological traits. Despite this lack of strict matching, SDE is maintained through functional guild complementarity: bats act as long-distance dispersal specialists, while civets provide niche coverage for the largest fruits. However, the aggregated seed clumps deposited by civets remain a concern for recruitment. These findings show that generalist interactions, supported by complementary guild functions, underpin effective seed dispersal. Conserving the full frugivore assemblage is therefore critical to sustaining ecological processes in botanical gardens and should directly inform faunal management strategies.

Article Details

Section

Articles

How to Cite

HANDAYANI, T. (2026) “Functional guild complementarity and morphological filtering in Annonaceae seed dispersal within a managed tropical garden”, Nusantara Bioscience, 18(1). doi:10.13057/nusbiosci/n180103.

References

Adyn MF, Sibarani MC, Utoyo L, Surya RA, Sedayu A. 2022. Role of siamang (Symphalangus syndactylus) as seed dispersal agent in a Sumatran lowland tropical forest. Biodiversitas 23 (4): 2101-2110. https://doi.org/10.13057/biodiv/d230445.

Ariati SR, Widyatmoko D. 2019. Bogor Botanic Gardens. Sibbaldia Intl J Bot Garden Hortic 17: 11-28. https://doi.org/10.24823/Sibbaldia. 2019.265.

Awaliah ATS, Dewi BS, Winarno GD. 2018. Palatabilitas badak sumatera (Dicerorhinus sumatrensis) di Suaka Rhino Sumatera. J Sylva Lestari 6 (3): 64-72. https://doi.org/10.23960/jsl3664-72. [Indonesian]

Aziz SA, McConkey KR, Tanalgo K, Sritongchuay T, Low MR, Yong JY, Mildenstein TL, Nuevo-Diego CE, Lim VC, Racey PA. 2021. The critical importance of old world fruit bats for healthy ecosystems and economies. Front Ecol Evol 9: 641411. https://doi.org/10.3389/fevo.2021.641411.

Cabral A, Bender IMA, Couvreur TLP, Faurby S, Hagen O, Hensen I, Kühn I, Rodrigues-Vaz C, Sauquet H, Tobias JA, Onstein RE. 2025. Seed-dispersing vertebrates and the abiotic environment shape functional diversity of the pantropical Annonaceae. New Phytol 246 (5): 2263-2279. https://doi.org/10.1111/nph.70113.

Campagnoli M, Christianini A, Peralta G. 2025. Plant and frugivore species characteristics drive frugivore contributions to seed dispersal effectiveness in a hyperdiverse community. Funct Ecol 39 (1): 238-253. https://doi.org/10.1111/1365-2435.14697.

Chen G, Sun W. 2018. The role of botanical gardens in scientific research, conservation, and citizen science. Plant Diver 40 (4): 181-188. https://doi.org/10.1016/j.pld.2018.07.006.

Coates-Estrada R, Estrada A. 1988. Frugivory and seed dispersal in Cymbopetalum baillonii (Annonaceae) at Los Tuxtlas, Mexico. J Trop Ecol 4 (2): 157-172. https://doi.org/10.1017/S0266467400002650.

Corlett RT. 2017. Frugivory and seed dispersal by vertebrates in tropical and subtropical Asia: An update. Glob Ecol Conserv 11: 1-22. https://doi.org/10.1016/j.gecco.2017.04.007.

Couvreur TLP, Maas PJM, Meinke S, Johnson DM, Keßler PJ. 2012. Keys to the genera of Annonaceae. Bot J Linn Soc 169 (1): 74-83. https://doi.org/10.1111/j.1095-8339.2012.01230.x.

Duan Q, Goodale E, Quan RC. 2014. Bird fruit preferences match the frequency of fruit colors in tropical Asia. Sci Rep 4: 5627. https://doi.org/10.1038/srep05627.

Fleming TH, Kress WJ. 2011. A brief history of fruits and frugivores. Acta Oecol 37 (6): 521-530. https://doi.org/10.1016/j.actao.2011.01.016.

Forget PM, Jordano P, Lambert JE, Böhning-Gaese K, Traveset A. 2011. Frugivores and seed dispersal (1985-2010); the 'seeds' dispersed, established, and matured. Acta Oecol 37: 517-520. https://doi.org/10.1016/j.actao.2011.09.008.

Fuzessy LF, Janson C, Silveira FA. 2018. Effects of seed size and frugivory degree on dispersal by Neotropical frugivores. Acta Oecol 93: 41-47. https://doi.org/10.1016/j.actao.2018.10.004.

Galetti M, Guevara R, Côrtes MC, Fadini R, Matter SV, Leite AB, Labecca F, Ribeiro T, Carvalho CS, Collevatti RG, Pires MM, Guimarães Jr PR, Brancalion PH, Ribeiro MC, Jordano P. 2013. Functional extinction of birds drives rapid evolutionary changes in seed size. Science 340 (6136): 1086-90. https://doi.org/10.1126/science.1233774.

Gautier-Hion A, Duplantier JM, Quris R, Feer F, Sourd C, Decoux JP, Dubost G, Emmons L, Erard C, Hecketsweiler P, Moungazi A, Roussilhon C, Thiollay JM. 1985. Fruit characters as a basis of fruit choice and seed dispersal in a tropical forest vertebrate community. Oecologia 65 (3): 324-337. https://doi.org/10.1007/BF00378906.

Girmay M. 2023. Roles of botanical gardens for conservation and requirements for their establishment: Review. Daagu Intl J Basic Appl Res 5: 182-192. https://doi.org/10.20372/dijbar.81657.

Handayani T. 2022. Pemencaran Biji Jenis-Jenis Tanaman Suku Annonaceae di Kebun Raya Bogor, Indonesia. Prosiding Seminar Nasional Masyarakat Biodiversitas Indonesia 8 (2): 136-141. https://doi.org/10.13057/psnmbi/m080205. [Indonesian]

Herrera CM. 2002. Seed dispersal by vertebrates. In: Herrera CM, Pellmyr O (eds.). Plant-Animal Interactions. An Evolutionary Approach. Blackwell Science, Oxford, UK.

Heywood VH. 2011. The role of botanic gardens as resource and introduction centres in the face of global change. Biodiver Conserv 20: 221-239. https://doi.org/10.1007/s10531-010-9781-5.

Hodgkison R, Balding ST, Zubaid A, Kunz TH. 2006. Fruit bats (Chiroptera: Pteropodidae) as seed dispersers and pollinators in a lowland Malaysian rain forest. Biotropica 35 (4): 491-502. https://doi.org/10.1111/j.1744-7429.2003.tb00606.x.

Howe HF, Smallwood J. 1982. Ecology of seed dispersal. Ann Rev Ecol Syst 13: 201-228. https://doi.org/10.1146/annurev.es.13.110182.001221.

Janzen D. H. 1985. On ecological fitting. Oikos 45 (3): 308-310. https://doi.org/10.2307/3565565.

Jordano P. 2000. Fruits and frugivory. In: Fenner M (eds.). Seeds: The Ecology of Regeneration in Plant Communities. 2nd ed. CABI Publisher, Wallingford, UK. https://doi.org/10.1079/9780851994321.0125.

Kissling WD, Rahbek C, Böhning-Gaese K. 2007. Food plant diversity as a broad-scale determinant of avian frugivore richness. Proc Biol Sci 274 (1611): 799-808. https://doi.org/10.1098/rspb.2006.0311.

Mahandran V, Murugan CM, Gang W, Jin C, Nathan PT. 2021. Multimodal cues facilitate ripe-fruit localization and extraction in free-ranging pteropodid bats. Behav Proces 189: 104426. https://doi.org/10.1016/j.beproc.2021.104426.

McConkey KR, Nathalang A, Brockelman WY, Saralamba C, Santon J, Matmoon U, Somnuk R, Srinoppawan K. 2018. Different megafauna varieties in their seed dispersal effectiveness of the megafaunal fruit Platymitra macrocarpa (Annonaceae). PLoS One 13 (7): e0198960. https://doi.org/10.1371/journal.pone.0198960.

McConkey KR, Prasad S, Corlett RT, Campos-Arceiz A, Brodie JF, Rogers H, Santamaria L. 2012. Review seed dispersal in changing landscapes. Biol Conserv 146 (1): 1-13. https://doi.org/10.1016/j/biocon.2011.09.018.

Melin AD, Nevo O, Shirasu M, Williamson RE, Garrett EC, Endo M, Sakurai K, Matsushita Y, Touhara K, Kawamura S. 2019. Fruit scent and observer color vision shape food-selection strategies in wild capuchin monkeys. Nat Commun 10 (1): 2407. https://doi.org/10.1038/s41467-019-10250-9.

Muscarella R, Fleming TH. 2007. The role of frugivorous bats in tropical forest succession. Biol Rev Camb Philos Soc 82 (4): 573-590. https://doi.org/10.1111/j.1469-185X.2007.00026.x.

Nakashima Y, Inoue E, Inoue-Murayama M, Sukor JRA. 2010. Functional uniqueness of a small carnivore as a seed dispersal agent: A case study of the common palm civets in the Tabin Wildlife Reserve, Sabah, Malaysia. Oecologia 164 (3): 721-730. https://doi.org/10.1007/s00442-010-1714-1.

Nakashima Y, Sukor JA. 2010. Importance of common palm civets (Paradoxurus hermaphroditus) as long-distance dispersers for large-seeded plants in degraded forests. Tropics 18 (4): 221-229. https://doi.org/10.3759/tropics.18.221.

Onstein RE, Kissling WD, Chatrou LW, Couvreur TLP, Morlon H, Sauquet H. 2019. Which frugivory-related traits facilitated historical long-distance dispersal in the custard apple family (Annonaceae)? J Biogeogr 46 (8): 1874-1888. https://doi.org/10.1111/jbi.13552.

Partasasmita R, Mardiastuti AN, Solihin DD, Widjajakusumah R, Prijono SN. 2017. Frugivorous birds are characteristic of seed dispersers in the shrubland tropical forest of West Java, Indonesia. Biodiversitas 18 (1): 263-268. https://doi.org/10.13057/biodiv/d180134.

Partasasmita R. 2015. The role of frugivorous birds in the dispersal of shrubs in the submontane zone of tropical forest, West Java, Indonesia. Nusantara Biosci 7 (2): 144-148. https://doi.org/10.13057/nusbiosci/n070214.

Primack RB, Miller-Rushing AJ. 2009. The role of botanical gardens in monitoring plant responses to climate change. New Phytol 182 (2): 30-313. https://doi.org/10.1111/j.1469-8137.2009.02712.x.

Ranuntu RA, Mallombasang SN. 2015. Studi populasi dan habitat anoa (Bubalus sp.) di Kawasan Hutan Lindung Desa Sangginora Kabupaten Poso. e-Jurnal Mitra Sains 3 (2): 81-94. [Indonesian]

Russo SE, Portnoy S, Augspurger CK. 2006. Incorporating animal behavior into seed dispersal models: implications for seed shadows. Ecology 87 (12): 3160-3174. https://doi.org/10.1890/0012-9658(2006)87[3160:IABISD]2.0.CO;2.

Safarinanugraha D, Gunawan A, Mugnisjah WQ. 2018. The development of Bogor Botanic Garden Design from 1817 to 2017 is based on spatial and functional considerations. IOP Conf Ser Earth Environ Sci 179: 012026. https://doi.org/10.1088/1755-1315/179/1/012026.

Saunders RMK. 2020. The evolution of key functional floral traits in the early-divergent angiosperm family Annonaceae. J Syst Evol 58 (4): 369-392. https://doi.org/10.1111/jse.12645.

Schupp W, Jordano P, Gómez JM. 2010. Seed dispersal effectiveness revisited: A conceptual review. New Phytol 188 (2): 333-353. https://doi.org/10.1111/j.1469-8137.2010.03402.x.

Soegiharto S, Kartono AP, Maryanto I. 2010. Pengelompokan kelelawar pemakan buah dan nektar berdasarkan karakteristik jenis pakan polen di Kebun Raya Bogor, Indonesia. Jurnal Biologi Indonesia 6 (2): 225-235. https://doi.org/10.47349/06022010/225. [Indonesian]

Steele MA, Yi X. 2020. Squirrel-seed interactions: The evolutionary strategies and impact of squirrels as both seed predators and seed dispersers. Front Ecol Evol 8: 259. https://doi.org/10.3389/fevo.2020.00259.

Subrata SA, Syahbudin A. 2016. The common palm civet is a potential seed disperser of important plant species in Java. AIP Conf Proc 1744: 020053. https://doi.org/10.1063/1.4953527.

Tsuji Y, Tatewaki T, Farajallah A, Tanaka H, Widayati KA, Suryobroto B. 2024. Food habits of the common palm civet (Paradoxurus hermaphroditus) in Pangandaran Nature Reserve, West Java, Indonesia: A preliminary report. Hayati J Biosci 31 (4): 687-692. https://doi.org/10.4308/hjb.31.4.687-692.

van Setten AK, Koek-Noorman J. 1992. Fruits and seeds of Annonaceae. Morphology and its significance for classification (Studies in Annonaceae XVII). Bibliothec Bot Heft: 142. https://www.schweizerbart.de/publications/detail/isbn/9783510480135/Bibliotheca_Botanica_Heft_142.

Wang G, Huang Y, Yao W, Huang Q, Huang Y, Wei L, Zhou Q. 2023. Structure and characteristics of the plant-frugivore bird network from the Guilin Botanical Garden. PeerJ 11: e15028. https://doi.org/10.7717/peerj.15028.

Wheelwright NT, Janson CH. 1985. Colors of fruit displays of bird-dispersed plants in two tropical forests. Am Nat 126 (6): 777-799. https://doi.org/10.1086/284453.