Recruitment bottleneck in aphyllous vanilla seedlings facing drought conditions

Authors

DOI:

https://doi.org/10.15517/rwsfdp60

Keywords:

aridity, deforestation, orchids, protocorm, seedling establishment, seedling mortality

Abstract

Seedling survival is strongly dependent on forest environmental conditions, which in Madagascar have been heavily degraded. Rising temperatures and declining rainfall further exacerbate the vulnerability of these ecosystems. We investigated seedling recruitment across ecologically diverse sites to identify the key factors influencing germination and seedling survival in aphyllous Vanilla species. In situ seedling monitoring and in vitro seed germination trials were conducted to assess tolerance to water stress at various developmental stages. Among the 13 study sites, only three showed positive recruitment rates, with two sites exhibiting rates exceeding 50%. Recruitment was influenced by factors such as fruiting success, soil acidity, high silt content, and clay-rich soil composition. After 12 months of monitoring, approximately 85% of seedlings were lost following severe drought conditions. In vitro asymbiotic germination assays revealed two distinct peaks: rapid germination of immature white seeds after four months, followed by delayed germination of mature black seeds eight months later. The assessment of drought tolerance across protocorm developmental stages exposed to a high-concentration gelling agent revealed that advanced-stage protocorms had increased resistance to water stress. However, no developmental stage was capable of surviving a prolonged six-month drought. Due to the absence of seedling recruitment in several locations, aphyllous vanilla recruitment may benefit from assisted propagation through seed cultures and the subsequent reintroduction of young plantlets into natural habitats. Moreover, conservation and restoration programs should incorporate research on developing soil conditions that facilitate vanilla seedling recruitment. 

Downloads

Download data is not yet available.

References

Abeli, T., Jäkäläniemi, A., Wannas, L., Mutikainen, P., & Tuomi, J. (2013). Pollen limitation and fruiting failure related to canopy closure in Calypso bulbosa (Orchidaceae), a northern food-deceptive orchid with a single flower. Botanical Journal of the Linnean Society, 171(4), 744–750. https://doi.org/10.1111/boj.12014

Ackerman, J. D., Sabat, A., & Zimmerman, J. K. (1996). Seedling establishment in an epiphytic orchid: an experimental study of seed limitation. Oecologia, 106, 192–198. https://doi.org/10.1007/BF00328598

Ackerman J.D. (2021). Orchids on the move: go forth & proliferate! In: Wang Y-T, Chang Y-CA, Lee Y-I, Chen F-C, Tsai W-C (Eds.), Proceedings of the 2021 Virtual World Orchid Conference (pp. 262–266). Tainan City: Taiwan Orchid Growers Association.

Allorge-Boiteau, L. (2005). Les vanilles succulentes de Madagascar. Succulentes, 2, 3–11.

Allorge-Boiteau, L. (2013). Une nouvelle espèce de vanille à Madagascar. Hommes Et Plantes, 85, 4–5.

Andriamihaja, C. F., Botomanga, A., Misandeau, C., Ramarosandratana, A. V, Grisoni, M., Da Silva, D., & Besse, P. (2022). Integrative taxonomy and phylogeny of leafless Vanilla orchids from the South‐West Indian Ocean region reveal two new Malagasy species. Journal of Systematics and Evolution, 61(1), 80–98. https://doi.org/10.1111/jse.12858

Andriamihaja, C.F., Ramarosandratana, A.V., Grisoni, M., Jeannoda, V.H., Besse, P., (2021). Drivers of population divergence and species differentiation in a recent group of indigenous orchids (Vanilla spp.) in Madagascar. Ecology Evolution, 11, 2681–2700. https://doi.org/10.1002/ECE3.7224.

Andriamihaja, C. F., Ramarosandratana, A. V., Grisoni, M., Jeannoda, V., & Besse, P. (2020). The leafless Vanilla species-complex from the south-west Indian ocean region: A taxonomic puzzle and a model for orchid evolution and conservation research. Diversity, 12(12), 1–25. https://doi.org/10.3390/D12120443

Arditti, J., & Ghani, A. K. A. (2000). Numerical and physical properties of orchid seeds and their biological implications. The New Phytologist, 145(3), 367–421. doi:10.1046/j.1469-8137.2000.00587.x

Bahadur, A., Batool, A., Nasir, F., Jiang, S., Mingsen, Q., Zhang, Q., Pan, J., Liu, Y., & Feng, H. (2019). Mechanistic insights into arbuscular mycorrhizal fungi-mediated drought stress tolerance in plants. International Journal of Molecular Sciences, 20(17), 4199. https://doi.org/10.3390/ijms20174199

Batty, A. L., Dixon, K. W., Brundrett, M., & Sivasithamparam, K. (2001). Constraints to symbiotic germination of terrestrial orchid seed in a mediterranean bushland. New Phytologist, 152(3), 511–520. https://doi.org/10.1046/j.0028-646X.2001.00277.x

Bazalar, V. P. F. (2020). Effects of water deficit on the physiology, biochemistry and morphology of the protocorms of the epiphytic orchid Laelia lobata Lindl. Phd Thesis. Universidade de São Paulo.

Bell, S. A. J. (2021). Successful recruitment following translocation of a threatened terrestrial orchid (Diuris tricolor) into mining rehabilitation in the Hunter Valley of NSW. Ecological Management & Restoration, 22(2), 204–207. https://doi.org/10.1111/emr.12473

Berry, A. S. F., Salazar-Sánchez, R., Castillo-Neyra, R., Borrini-Mayori, K., Chipana-Ramos, C., Vargas-Maquera, M., Ancca-Juarez, J., Náquira-Velarde, C., Levy, M., & Brisson, D. (2019). Sexual reproduction in a natural Trypanosoma cruzi population. PLoS Neglected Tropical Diseases, 13(5), e0007392. https://doi.org/10.1371/journal.pntd.0007392

Bewley, J. D., & Black, M. (2013). Germination, Structure, and Composition. In: Springer Science & Business Media (Eds), Seeds: physiology of development and germination (pp. 1–33). New York: Plenum Press. DOI 10.1007/978-1-4899-1002-8

Blagodatskaya, E. V, & Anderson, T.-H. (1998). Interactive effects of pH and substrate quality on the fungal-to-bacterial ratio and qCO2 of microbial communities in forest soils. Soil Biology and Biochemistry, 30(10–11), 1269–1274. https://doi.org/10.1016/S0038-0717(98)00050-9

Booy, G., Hendriks, R. J. J., Smulders, M. J. M., Van Groenendael, J. M., & Vosman, B. (2000). Genetic diversity and the survival of populations. Plant Biology, 2(04), 379–395.

Botomanga, A., Andriamihaja, C. F., Besse, P., Jeannoda, V. H., Grisoni, M., Ny Aina Ranaivoson, S. E. F., Antsonantenainarivony, G., Fuzzati, N., & Ramarosandratana, A. V. (2024a). Continuous Degradation of Forest Structure and Composition Causes a Shift in Phorophytes and Population Genetics in Aphyllous Vanilla Species. Tropical Conservation Science, 17. https://doi.org/10.1177/19400829241301920

Botomanga, A., Jeannoda, V. H., Fuzzati, N., & Ramarosandratana, A. V. (2024b). Morpho-anatomical responses of leafless Vanilla spp. roots to drought and habitat degradation. Flora, 152562. https://doi.org/10.1016/j.flora.2024.152562

Bouetard, A., Lefeuvre, P., Gigant, R., Bory, S., Pignal, M., Besse, P., & Grisoni, M. (2010). Evidence of transoceanic dispersion of the genus Vanilla based on plastid DNA phylogenetic analysis. Molecular Phylogenetics and Evolution, 55(2), 621–630. https://doi.org/10.1016/j.ympev.2010.01.021

Braun-Blanquet, J. (1932). Plant sociology. The study of plant communities. 1st ed. McGraw-Hill Book Co., Inc., New York and London

Cameron, K. M., & Chase, M. W. (1998). Seed morphology of vanilloid orchids (Vanilloideae: Orchidaceae). Lindleyana, 13(3), 148–169.

Capblancq, T., Munson, H., Butnor, J. R., & Keller, S. R. (2021). Genomic drivers of early-life fitness in Picea rubens. Conservation Genetics, 22(6), 963–976. https://doi.org/10.1007/s10592-021-01378-7

Cheng, S., Zou, Y.-N., Kuča, K., Hashem, A., Abd_Allah, E. F., & Wu, Q.-S. (2021). Elucidating the mechanisms underlying enhanced drought tolerance in plants mediated by arbuscular mycorrhizal fungi. Frontiers in Microbiology, 12, 809473. https://doi.org/10.3389/fmicb.2021.809473

Cornet, A. (1974). Essai de cartographie bioclimatique à Madagascar. Orstom Paris.

Cribb, P., & Hermans, J. (2009). Field guide to the orchids of Madagascar. Royal Botanic Gardens.

Dalling, J. W., Muller‐Landau, H. C., Wright, S. J., & Hubbell, S. P. (2002). Role of dispersal in the recruitment limitation of neotropical pioneer species. Journal of Ecology, 90(4), 714–727. https://doi.org/10.1046/j.1365-2745.2002.00706.x

Diez, J. M. (2007). Hierarchical patterns of symbiotic orchid germination linked to adult proximity and environmental gradients. Journal of Ecology, 95, 159–170. https://www.jstor.org/stable/4495966

Donque, G. (1972). The climatology of Madagascar. In: Battistini, R., Richard-Vindard, G. (Eds), Biogeography and ecology in Madagascar (pp. 87–144). Dordrecht: Springer. https://doi.org/10.1007/978-94-015-7159-3_3

Dunn, J. C., Asensio, N., Arroyo‐Rodríguez, V., Schnitzer, S., & Cristóbal‐Azkarate, J. (2012). The ranging costs of a fallback food: liana consumption supplements diet but increases foraging effort in howler monkeys. Biotropica, 44(5), 705–714. https://doi.org/10.1111/j.1744-7429.2012.00856.x

Eriksson, O., & Ehrlén, J. (1992). Seed and microsite limitation of recruitment in plant populations. Oecologia, 91, 360–364. https://doi.org/10.1007/BF00317624

Evans, A., Janssens, S., & Jacquemyn, H. (2020). Impact of Climate Change on the Distribution of Four Closely Related Orchis (Orchidaceae) Species. Diversity, 12(8), 312. https://doi.org/10.3390/d12080312

Falara, V., Amarasinghe, R., Poldy, J., Pichersky, E., Barrow, R. A., & Peakall, R. (2013). The production of a key floral volatile is dependent on UV light in a sexually deceptive orchid. Annals of Botany, 111(1), 21–30. https://doi.org/10.1093/aob/mcs228

Fang, L., Kong, X., Wen, Y., Li, J., Yin, Y., Li, L., Ma, G., Wu, K., & Zeng, S. (2021). Characterization of embryo and protocorm development of Paphiopedilum spicerianum. Plant Physiology and Biochemistry, 167, 1024–1034. https://doi.org/10.1016/j.plaphy.2021.09.001

Fay, M. F. (2015). British and Irish orchids in a changing world. Curtis’s Botanical Magazine, 32(1), 3–23. https://www.jstor.org/stable/48505622

Fay, M. F., Pailler, T., & Dixon, K. W. (2015). Orchid conservation: making the links. Annals of Botany, 116(3), 377–379. https://doi.org/10.1093/aob/mcv142

Félix-Burruel, R. E., Larios, E., González, E. J., & Búrquez, A. (2025). Population decline of the saguaro cactus throughout its distribution is associated with climate change. Annals of Botany, 135(1–2), 317–328. https://doi.org/10.1093/aob/mcae094

Fernández, M., Kaur, J., & Sharma, J. (2023). Co-occurring epiphytic orchids have specialized mycorrhizal fungal niches that are also linked to ontogeny. Mycorrhiza, 33(1), 87–105. https://doi.org/10.1007/s00572-022-01099-w

Fick, S. E., & Hijmans, R. J. (2017). WorldClim 2: new 1‐km spatial resolution climate surfaces for global land areas. International Journal of Climatology, 37(12), 4302–4315. https://doi.org/10.1002/joc.5086

Flanagan, N. S., Chavarriaga, P., & Mosquera‐Espinosa, A. T. (2018). Conservation and sustainable use of Vanilla crop wild relatives in Colombia. Handbook of Vanilla Science and Technology, 85–109. https://doi.org/10.1002/9781119377320.ch6

Fritsche, Y., Pinheiro, M. V. M., & Guerra, M. P. (2022). Light quality and natural ventilation have different effects on protocorm development and plantlet growth stages of the in vitro propagation of Epidendrum fulgens (Orchidaceae). South African Journal of Botany, 146, 864–874. https://doi.org/10.1016/j.sajb.2022.02.019

Gale, S. W., Fischer, G. A., Cribb, P. J., & Fay, M. F. (2018). Orchid conservation: bridging the gap between science and practice. Botanical Journal of the Linnean Society, 186(4), 425–434. https://doi.org/10.1093/botlinnean/boy003

Gao, Y., Guo, S., & Xing, X. (2019). Fungal diversity and mechanisms of symbiotic germination of orchid seeds: a review. Mycosystema, 38(11), 1808–1825.

Garnier, S., Giordanengo, E., Saatkamp, A., Santonja, M., Reiter, I. M., Orts, J., Gauquelin, T., & Meineri, E. (2021). Amplified drought induced by climate change reduces seedling emergence and increases seedling mortality for two Mediterranean perennial herbs. Ecology and Evolution, 11(22), 16143–16152. https://doi.org/10.1002/ece3.8295

Gautier, L., Chatelain, C., & Spichiger, R.-E. (1994). Presentation of a releve method for vegetation studies based on high resolution satellite imagery. In: J. H. Seyani & A. C. Chikuni (Eds.), Proceedings of XIII th plenary meeting of AETFAT (pp. 1339–1350). National Herbarium and Botanic Gardens of Malawi.

Gebrechorkos, S. H., Sheffield, J., Vicente-Serrano, S. M., Funk, C., Miralles, D. G., Peng, J., Dyer, E., Talib, J., Beck, H. E., & Singer, M. B. (2025). Warming accelerates global drought severity. Nature, 1–8. https://doi.org/10.1038/s41586-025-09047-2

Gigant, R. L., De Bruyn, A., Church, B., Humeau, L., Gauvin-Bialecki, A., Pailler, T., Grisoni, M., & Besse, P. (2014). Active sexual reproduction but no sign of genetic diversity in range-edge populations of Vanilla roscheri Rchb. f.(Orchidaceae) in South Africa. Conservation Genetics, 15(6), 1403–1415. https://doi.org/10.1007/s10592-014-0626-8

Gill, D. E. (1996). The natural population ecology of temperate terrestrials: Pink lady’s slippers, Cypripedium acaule. North American Native Terrestrial Orchids conference: Propagation and Production, 91–106.

Godron, M., Daget, P., Long, G., Sauvage, C., Emberger, L., Le Gloch, E., Poissonnet, J., & Wacquant, J. P. (1983). Relevé méthodologique de la végétation et du milieu, code et transcription sur carte perforée. CNRS, Paris, 281p.

González-Orellana, N., Mendoza, A. S., Tremblay, R. L., & Ackerman, J. D. (2024). Host suitability for germination differs from that of later stages of development in a rare epiphytic orchid. Lankesteriana, 93–114. https://doi.org/10.15517/lank.v24i1.59617

Hankin, L. E., Barrios-Masias, F. H., Urza, A. K., & Bisbing, S. M. (2025). Lethal combination for seedlings: extreme heat drives mortality of drought-exposed high-elevation pine seedlings. Annals of Botany, 135(1–2), 293–304. https://doi.org/10.1093/aob/mcae064

Hempel, S., Götzenberger, L., Kühn, I., Michalski, S. G., Rillig, M. C., Zobel, M., & Moora, M. (2013). Mycorrhizas in the Central European flora: relationships with plant life history traits and ecology. Ecology, 94(6), 1389–1399. https://doi.org/10.1890/12-1700.1

Hending, D., Holderied, M., McCabe, G., & Cotton, S. (2022). Effects of future climate change on the forests of Madagascar. Ecosphere, 13(4), e4017. https://doi.org/10.1002/ecs2.4017

Hens, H., Pakanen, V.-M., Jäkäläniemi, A., Tuomi, J., & Kvist, L. (2017). Low population viability in small endangered orchid populations: Genetic variation, seedling recruitment and stochasticity. Biological Conservation, 210, 174–183. https://doi.org/10.1016/j.biocon.2017.04.019

Herrera, H., García-Romera, I., Meneses, C., Pereira, G., & Arriagada, C. (2019). Orchid mycorrhizal interactions on the Pacific side of the Andes from Chile. A review. Journal of Soil Science and Plant Nutrition, 19, 187–202. https://doi.org/10.1007/s42729-019-00026-x

Higaki, K., Rammitsu, K., Yamashita, Y., Yukawa, T., & Ogura-Tsujita, Y. (2017). A method for facilitating the seed germination of a mycoheterotrophic orchid, Gastrodia pubilabiata, using decomposed leaf litter harboring a basidiomycete fungus, Mycena sp. Botanical Studies, 58, 1–7. https://doi.org/10.1186/s40529-017-0214-6

Horth, L. (2019). Understanding the impact of plant–arthropod interactions, pollination, and canopy light on the rare orchid, small whorled pogonia (Isotria medeoloides). Plant Ecology, 220, 563–576. https://doi.org/10.1007/s11258-019-00936-x

Hothorn, T., Bretz, F., & Westfall, P. (2015). Package multcomp: Simultaneous Inference in General Parametric Models. Published Online in the CRAN Repository.

Huang, H., & Song, S. (2013). Change in desiccation tolerance of maize embryos during development and germination at different water potential PEG-6000 in relation to oxidative process. Plant Physiology and Biochemistry, 68, 61–70. https://doi.org/10.1016/j.plaphy.2013.02.029

Huntley, B. J. (2023). Soil, water and nutrients. In Ecology of Angola: Terrestrial biomes and ecoregions. Springer, 127–147. https://doi.org/10.1007/978-3-031-18923-4_6

Izuddin, M., Yam, T. W., & Webb, E. L. (2019). Germination niches and seed persistence of tropical epiphytic orchids in an urban landscape. Journal of Plant Research, 132(3), 383–394. https://doi.org/10.1007/s10265-019-01110-0

Jaganathan, G. K., Li, J., Biddick, M., Han, K., Song, D., Yang, Y., Han, Y., & Liu, B. (2019). Mechanisms underpinning the onset of seed coat impermeability and dormancy-break in Astragalus adsurgens. Scientific Reports, 9(1), 9695. https://doi.org/10.1038/s41598-019-46158-z

Janissen, B., Lawrie, A. C., & Huynh, T. (2022). Warm stratification and optimised temperatures improve conservation of the endangered orchid, Caladenia robinsonii (Orchidaceae). Australian Journal of Botany, 70(4), 275–291. https://doi.org/10.1071/BT21085

Janowski, D., & Leski, T. (2022). Factors in the distribution of mycorrhizal and soil fungi. Diversity, 14(12), 1122. https://doi.org/10.3390/d14121122

Jolman, D., Batalla, M. I., Hungerford, A., Norwood, P., Tait, N., & Wallace, L. E. (2022). The challenges of growing orchids from seeds for conservation: An assessment of asymbiotic techniques. Applications in Plant Sciences, 10(5), e11496. https://doi.org/10.1002/aps3.11496

Kartzinel, T. R., Trapnell, D. W., & Shefferson, R. P. (2013). Critical importance of large native trees for conservation of a rare Neotropical epiphyte. Journal of Ecology, 101(6), 1429–1438. https://doi.org/10.1111/1365-2745.12145

Kassambara, A., & Mundt, F. (2017). Package ‘factoextra.’ Extract and Visualize the Results of Multivariate Data Analyses, 76(2). Published Online in the CRAN Repository

Kinderen, G. van der. (1995). A method for the study of field germinated seeds of terrestrial orchids. Lindleyana, 10 (2), 68–73

Kindlmann, P., Meléndez-Ackerman, E. J., & Tremblay, R. L. (2014). Disobedient epiphytes: colonization and extinction rates in a metapopulation of Lepanthes rupestris (Orchidaceae) contradict theoretical predictions based on patch connectivity. Botanical Journal of the Linnean Society, 175(4), 598–606. https://doi.org/10.1111/boj.12180

Kirillova, I. A., & Kirillov, D. V. (2020). Effect of illumination conditions on the reproductive success of Epipactis helleborine (L.) Crantz (Orchidaceae). Russian Journal of Ecology, 51, 389–393. https://doi.org/10.1134/S1067413620040098

Kirillova, I. A., & Kirillov, D. V. (2019). Effect of lighting conditions on the reproductive success of Cypripedium calceolus L. (Orchidaceae, Liliopsida). Biology Bulletin, 46, 1317–1324. https://doi.org/10.1134/S1062359019100157

Kleyheeg, E., Claessens, M., & Soons, M. B. (2018). Interactions between seed traits and digestive processes determine the germinability of bird-dispersed seeds. PLoS One, 13(4), e0195026. https://doi.org/10.1371/journal.pone.0195026

Klimaszewska, K., Bernier-Cardou, M., Cyr, D. R., & Sutton, B. C. S. (2000). Influence of gelling agents on culture medium gel strength, water availability, tissue water potential, and maturation response in embryogenic cultures of Pinus strobus L. In Vitro Cellular & Developmental Biology-Plant, 36, 279–286. https://doi.org/10.1007/s11627-000-0051-1

Klimaszewska, K., & Smith, D. R. (1997). Maturation of somatic embryos of Pinus strobus is promoted by a high concentration of gellan gum. Physiologia Plantarum, 100(4), 949–957. https://doi.org/10.1111/j.1399-3054.1997.tb00022.x

Kumari, N., & Mohan, C. (2021). Basics of clay minerals and their characteristic properties. In: Gustavo Morari Do Nascimento (Ed.), Clay and Clay Minerals (pp 15–43). London: IntechOpen. DOI: 10.5772/intechopen.97672

Lê, S., Josse, J., & Husson, F. (2008). FactoMineR: an R package for multivariate analysis. Journal of Statistical Software, 25, 1–18.

Lee, Y.-I., Chung, M.-C., Yeung, E. C., & Lee, N. (2015). Dynamic distribution and the role of abscisic acid during seed development of a lady’s slipper orchid, Cypripedium formosanum. Annals of Botany, 116(3), 403–411. https://doi.org/10.1093/aob/mcv079

Li, J., Ramirez, G. H., Kiani, M., Quideau, S., Smith, E., Janzen, H., Larney, F., & Puurveen, D. (2018). Soil organic matter dynamics in long-term temperate agroecosystems: Rotation and nutrient addition effects. Canadian Journal of Soil Science, 98(2), 232–245. https://doi.org/10.1139/cjss-2017-0127

Li, T., Yang, W., Selosse, M.-A., & Gao, J. (2021). Progress and prospects of mycorrhizal fungal diversity in orchids. Frontiers in Plant Science, 12, 646325. https://doi.org/10.3389/fpls.2021.646325

Li, Y.-Y., Boeraeve, M., Cho, Y.-H., Jacquemyn, H., & Lee, Y.-I. (2022). Mycorrhizal switching and the role of fungal abundance in seed germination in a fully mycoheterotrophic orchid, Gastrodia confusoides. Frontiers in Plant Science, 12, 775290. https://doi.org/10.3389/fpls.2021.775290

Madre, Jean François (2011). Mesurim un logiciel destiné à faire différents types de travaux sur les images numérisées, ENS, ACCES, Lyon, France. https://svt.ac-amiens.fr/040-vue-d-ensemble-des-logiciels-de-m-madre.html

Mahdavi, Z., Daylami, S. D., Fadavi, A., & Vahdati, K. (2023). Artificial seed production of Phalaenopsis orchid: effect of encapsulation materials, temperature, light spectra, and storage period. Plant Cell, Tissue and Organ Culture, 155(3), 797–808. https://doi.org/10.1007/s11240-023-02600-9

Matus, F. J. (2021). Fine silt and clay content is the main factor defining maximal C and N accumulations in soils: a meta-analysis. Scientific Reports, 11(1), 6438. https://doi.org/10.1038/s41598-021-84821-6

Maxted, N., & Kell, S. P. (2009). Establishment of a global network for the in situ conservation of crop wild relatives: status and needs. FAO Commission on Genetic Resources for Food and Agriculture, Rome, Italy, 266.

McCormick, M. K., Lee Taylor, D., Juhaszova, K., Burnett, R. K., Whigham, D. F., & O’Neill, J. P. (2012). Limitations on orchid recruitment: Not a simple picture. Molecular Ecology, 21(6), 1511–1523. https://doi.org/10.1111/j.1365-294X.2012.05468.x

McCormick, M. K., Parker, K. L., Szlavecz, K., & Whigham, D. F. (2013). Native and exotic earthworms affect orchid seed loss. AoB Plants, 5, plt018. https://doi.org/10.1093/aobpla/plt018

McCormick, M. K., & Jacquemyn, H. (2014). What constrains the distribution of orchid populations? New Phytologist, 202(2), 392–400. https://doi.org/10.1111/nph.12639

McCormick, M. K., Taylor, D. L., Whigham, D. F., & Burnett Jr, R. K. (2016). Germination patterns in three terrestrial orchids relate to abundance of mycorrhizal fungi. Journal of Ecology, 104(3), 744–754. https://doi.org/10.1111/1365-2745.12556

McCormick, M. K., Whigham, D. F., & Canchani‐Viruet, A. (2018). Mycorrhizal fungi affect orchid distribution and population dynamics. New Phytologist, 219(4), 1207–1215. https://doi.org/10.1111/nph.15223

Midgley, G. F., & Vander Heyden, F., (1999). Form and function in perennial plants. In: Dean, W. R. J., Milton, S. J. (Eds.), The Karoo: Ecological Patterns and Processes (pp. 90–106). Cambridge, Cambridge University Press.

Milton, S. J., Clark, C., Hundermark, C. R., Hurt, C., & Van der Merwe, H. (2024). Population trends in an endemic dwarf succulent over two decades: rainfall, elevation, microsite and landuse effects. Journal of Arid Environments, 223, 105181. https://doi.org/10.1016/j.jaridenv.2024.105181

Moat, J., & Smith, P. P. (2007). Atlas of the vegetation of Madagascar. Royal Botanic Gardens, Kew.

Montgomery, G. G., & M. E. Sunquist., (1978). Habitat selection and use by two-toed and three-toed sloths. In: G. G. Montgomery (Eds), The ecology of arboreal foliovores (pp. 329–359). Smithsonian Institution Press, Washing-ton, D.C., USA.

Moreno-Maroto, J. M., & Alonso-Azcárate, J. (2018). What is clay? A new definition of “clay” based on plasticity and its impact on the most widespread soil classification systems. Applied Clay Science, 161, 57–63. https://doi.org/10.1016/j.clay.2018.04.011

Muñoz-Rojas, M., Erickson, T. E., Martini, D. C., Dixon, K. W., & Merritt, D. J. (2016). Climate and soil factors influencing seedling recruitment of plant species used for dryland restoration. Soil, 2(2), 287–298. https://doi.org/10.5194/soil-2-287-2016

Murashige, T., & Skoog, F. (1962). A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiologia Plantarum, 15(3).

Nathan, R., & Muller-Landau, H. C. (2000). Spatial patterns of seed dispersal, their determinants and consequences for recruitment. Trends in Ecology & Evolution, 15(7), 278–285. DOI: 10.1016/S0169-5347(00)01874-7

Nishimura, G., & Tamura, M. (1993). Seed coat formation in Apostasia nipponica. Journal of Japanese Botany, 68(4) Doi:10.5555/19940311215

Ntuli, T. M. (2012). Drought and desiccation-tolerance and sensitivity in plants. In: John Mworia (Ed.), Botany (pp. 29–60). Croatie: InTech.

Owens, L. D., & Wozniak, C. A. (1991). Measurement and effects of gel matric potential and expressibility on production of morphogenic callus by cultured sugarbeet leaf discs. Plant Cell, Tissue and Organ Culture, 26, 127–133. https://doi.org/10.1007/BF00036116

Paulo, D., Diekmann, O., Ramos, A. A., Alberto, F., & Serrão, E. A. (2019). Sexual reproduction vs. clonal propagation in the recovery of a seagrass meadow after an extreme weather event. Scientia Marina, 83(4), 357–363. https://doi.org/10.3989/scimar.04843.06A

Pauwels, R., Graefe, J., & Bitterlich, M. (2023). An arbuscular mycorrhizal fungus alters soil water retention and hydraulic conductivity in a soil texture specific way. Mycorrhiza, 33(3), 165–179. https://doi.org/10.1007/s00572-023-01106-8

Petersson, L. (2015). Pollination biology of the endemic orchid Vanilla bosseri in Madagascar. Master Thesis. Uppsala University, Disciplinary Domain of Science and Technology, Biology Education Center.

Petrolli, R., Zinger, L., Perez‐Lamarque, B., Collobert, G., Griveau, C., Pailler, T., Selosse, M., & Martos, F. (2022). Spatial turnover of fungi and partner choice shape mycorrhizal networks in epiphytic orchids. Journal of Ecology, 110(11), 2568–2584. https://doi.org/10.1111/1365-2745.13986

Phillips, R. D., Reiter, N., & Peakall, R. (2020). Orchid conservation: from theory to practice. Annals of Botany, 126(3), 345–362. https://doi.org/10.1093/aob/mcaa093

Pimentel, D., Wilson, C., McCullum, C., Huang, R., Dwen, P., Flack, J., Tran, Q., Saltman, T., & Cliff, B. (1997). Economic and environmental benefits of biodiversity. BioScience, 47(11), 747–757. https://doi.org/10.2307/1313097

Poggio, L., De Sousa, L. M., Batjes, N. H., Heuvelink, G. B. M., Kempen, B., Ribeiro, E., & Rossiter, D. (2021). SoilGrids 2.0: producing soil information for the globe with quantified spatial uncertainty. Soil, 7(1), 217–240. https://doi.org/10.5194/soil-7-217-2021

Porras-Alfaro, A., & Bayman, P. (2007). Mycorrhizal fungi of Vanilla: diversity, specificity and effects on seed germination and plant growth. Mycologia, 99(4), 510–525. https://doi.org/10.1080/15572536.2007.11832545

Portères, R. (1954). Le genre Vanilla et ses espèces : Le Vanillier et la Vanille dans le Monde. Encyclopedia of Biology, 46, 94–290.

Prutsch, J., Schardt, A., & Schill, R. (2000). Adaptations of an orchid seed to water uptake and-storage. Plant Systematics and Evolution, 220, 69–75. https://doi.org/10.1007/BF00985371

Rabot, E., Wiesmeier, M., Schlüter, S., & Vogel, H.-J. (2018). Soil structure as an indicator of soil functions: A review. Geoderma, 314, 122–137. https://doi.org/10.1016/j.geoderma.2017.11.009

Rafanoharana, S. C., Andrianambinina, F. O. D., Rasamuel, H. A., Waeber, P. O., Wilmé, L., & Ganzhorn, J. U. (2024). Projecting forest cover in Madagascar’s protected areas to 2050 and its implications for lemur conservation. Oryx, 58(2), 155–163. https://doi.org/10.1017/S0030605323001175

Rakotoarivelo, N. H., Randrianarivony, T. N., Rakotoarivony, F., & Randrianasolo, A. (2019). “Mangidy”: Malagasy Folk Beverages Sold in Madagascar’s Market Places. Ethnobotany Research and Applications, 18, 1–14. https://ethnobotanyjournal.org/index.php/era/article/view/1565

Randriamarolaza, L. Y. A., Aguilar, E., Skrynyk, O., Vicente‐Serrano, S. M., & Domínguez‐Castro, F. (2022). Indices for daily temperature and precipitation in Madagascar, based on quality‐controlled and homogenized data, 1950–2018. International Journal of Climatology, 42(1), 265–288. https://doi.org/10.1002/joc.7243

Randriamiharisoa, M. N., Kuhlman, A. R., Jeannoda, V., Rabarison, H., Rakotoarivelo, N., Randrianarivony, T., Raktoarivony, F., Randrianasolo, A., & Bussmann, R. W. (2015). Medicinal plants sold in the markets of Antananarivo, Madagascar. Journal of Ethnobiology and Ethnomedicine, 11, 1–13. https://doi.org/10.1186/s13002-015-0046-y

Rasmussen, H. N. (1992). Seed dormancy patterns in Epipactis palustris (Orchidaceae): Requirements for germination and establishment of mycorrhiza. Physiologia Plantarum, 86(1), 161–167. https://doi.org/10.1111/j.1399-3054.1992.tb01325.x

Rasmussen, H. N., Dixon, K. W., Jersáková, J., & Těšitelová, T. (2015). Germination and seedling establishment in orchids: a complex of requirements. Annals of Botany, 116(3), 391–402.

Rasmussen, H. N., & Whigham, D. F. (1998). Importance of woody debris in seed germination of Tipularia discolor (Orchidaceae). American Journal of Botany, 85(6), 829–834. https://doi.org/10.2307/2446418

R Core Team (2023). R: A Language and Environment for Statistical Computing_. R Foundation for Statistical Computing, Vienna, Austria. <https://www.R-project.org/>.

Read, D. J., Haggar, J., Magkourilou, E., Durant, E., Johnson, D., Leake, J. R., & Field, K. J. (2024). Photosynthate transfer from an autotrophic orchid to conspecific heterotrophic protocorms through a common mycorrhizal network. New Phytologist, 243(1), 398–406. https://doi.org/10.1111/nph.19810

Rendigs, A., Radespiel, U., Wrogemann, D., & Zimmermann, E. (2003). Relationship between microhabitat structure and distribution of mouse lemurs (Microcebus spp.) in northwestern Madagascar. International Journal of Primatology, 24, 47–64. https://doi.org/10.1023/A:1021494428294

Ripley, B. S., Abraham, T., Klak, C., & Cramer, M. D. (2013). How succulent leaves of Aizoaceae avoid mesophyll conductance limitations of photosynthesis and survive drought. Journal of Experimental Botany, 64(18), 5485–5496. https://doi.org/10.1093/jxb/ert314

Ravelonanosy R., Andriamihaja C., Grisoni M., Ramarosandratana A. V., Rafidison V., Fuzzati N., Besse P. (2025). Leafless Vanilla species from Madagascar as potential models to study bioclimatic adaptation. In: Tikam Dakal (Ed.), Advances in Genetic Diversity - Recent Advancements, Challenges and Prospects. IntechOpen. DOI: 10.5772/intechopen.1012448

Rousk, J., Bååth, E., Brookes, P. C., Lauber, C. L., Lozupone, C., Caporaso, J. G., Knight, R., & Fierer, N. (2010). Soil bacterial and fungal communities across a pH gradient in an arable soil. The ISME Journal, 4(10), 1340–1351. https://doi.org/10.1038/ismej.2010.58

Salgotra, R. K., & Chauhan, B. S. (2023). Genetic diversity, conservation, and utilization of plant genetic resources. Genes, 14(1), 174. https://doi.org/10.3390/genes14010174

Sathiyadash, K., Muthukumar, T., Karthikeyan, V., & Rajendran, K. (2020). Orchid mycorrhizal fungi: structure, function, and diversity. Orchid Biology: Recent Trends & Challenges, 239–280. https://doi.org/10.1007/978-981-32-9456-1_13

Scade, A., Brundrett, M. C., Batty, A. L., Dixon, K. W., & Sivasithamparam, K. (2006). Survival of transplanted terrestrial orchid seedlings in urban bushland habitats with high or low weed cover. Australian Journal of Botany, 54(4), 383–389. https://doi.org/10.1071/BT04025

Schneider, C. A., Rasband, W. S., & Eliceiri, K. W. (2012). NIH Image to ImageJ: 25 years of image analysis. Nature Methods, 9(7), 671–675. doi: 10.1038/nmeth.2089

Schoonheydt, R. A., Johnston, C. T., & Bergaya, F. (2018). Clay minerals and their surfaces. Developments in clay science, 9 (1), 1–21). https://doi.org/10.1016/B978-0-08-102432-4.00001-9

Shao, S.-C., Burgess, K. S., Cruse-Sanders, J. M., Liu, Q., Fan, X.-L., Huang, H., & Gao, J.-Y. (2017). Using in situ symbiotic seed germination to restore over-collected medicinal orchids in Southwest China. Frontiers in Plant Science, 8, 888. https://doi.org/10.3389/fpls.2017.00888

Shefferson, R. P., Jacquemyn, H., Kull, T., & Hutchings, M. J. (2020). The demography of terrestrial orchids: life history, population dynamics and conservation. Botanical Journal of the Linnean Society, 192(2), 315–332. https://doi.org/10.1093/botlinnean/boz084

Šoch, J., Šonka, J., & Ponert, J. (2023). Acid scarification as a potent treatment for an in vitro germination of mature endozoochorous Vanilla planifolia seeds. Botanical Studies, 64(1), 9. https://doi.org/10.1186/s40529-023-00374-z

Sorgato, J. C., Soares, J. S., Damiani, C. R., & Ribeiro, L. M. (2020). Effects of light, agar, activated charcoal, and culture medium on the germination and early development of’Dendrobium’seedlings. Australian Journal of Crop Science, 14(4), 557–564.

Sousa, K. C. I., Araújo, L. G. de, Silva, C. de S., Carvalho, J. C. B. de, Sibov, S. T., Gonçalves, L. de A., Pereira, M. C., Gonçalves, F. J., & Filippi, M. C. da C. de. (2019). Seed germination and development of orchid seedlings (Cyrtopodium saintlegerianum) with fungi. Rodriguésia, 70, e02302016. https://doi.org/10.1590/2175-7860201970004

Stuckey, I. H. (1967). Environmental factors and the growth of native orchids. American Journal of Botany, 54(2), 232–241. https://doi.org/10.1002/j.1537-2197.1967.tb06914.x

Suzzi-Simmons, A. (2023). Status of deforestation of Madagascar. Global Ecology and Conservation, 42, e02389. https://doi.org/10.1016/j.gecco.2023.e02389

Swarts, N. D., & Dixon, K. W. (2009). Terrestrial orchid conservation in the age of extinction. Annals of Botany, 104(3), 543–556. https://doi.org/10.1093/aob/mcp025

Tadross, M., Randriamarolaza, L., Rabefitia, Z., & Zheng, K. Y. (2008). Climate change in Madagascar; recent past and future. World Bank, Washington, DC, 18, 1771–1790.

Těšitelová, T., Klimešová, L., Vogt-Schilb, H., Kotilínek, M., & Jersáková, J. (2022). Addition of fungal inoculum increases germination of orchid seeds in restored grasslands. Basic and Applied Ecology, 63, 71–82. https://doi.org/10.1016/j.baae.2022.04.001

Timsina, B., Rokaya, M. B., Münzbergová, Z., Kindlmann, P., Shrestha, B., Bhattarai, B., & Raskoti, B. B. (2016). Diversity, distribution and host-species associations of epiphytic orchids in Nepal. Biodiversity and Conservation, 25, 2803–2819. https://doi.org/10.1007/s10531-016-1205-8

Weiskopf, S. R., Cushing, J. A., Morelli, T. L., & Myers, B. J. E. (2021). Climate change risks and adaptation options for Madagascar. Ecology and Society, 26(4), 36. https://doi.org/10.5751/ES-12816-260436

Wojtyla, Ł., Paluch-Lubawa, E., Sobieszczuk-Nowicka, E., & Garnczarska, M. (2020). Drought stress memory and subsequent drought stress tolerance in plants. In: Mohammad A. H., Fulai L., David J. B., Masayuki F., Bingru H. (Eds.), Priming-mediated stress and cross-stress tolerance in crop plants (pp. 115–131). Academic Press. https://doi.org/10.1016/B978-0-12-817892-8.00007-6

Wright, M., French, G., Cross, R., Cousens, R., Andrusiak, S., & McLean, C. B. (2007). Site amelioration for direct seeding of Caladenia tentaculata improves seedling recruitment and survival in natural habitat. Lankesteriana, 7(1–2), 430–432. https://doi.org/10.15517/lank.v7i1-2.19653

Xu, X., Fang, L., Li, L., Ma, G., Wu, K., & Zeng, S. (2020). Abscisic acid inhibits asymbiotic germination of immature seeds of Paphiopedilum armeniacum. International Journal of Molecular Sciences, 21(24), 9561. https://doi.org/10.3390/ijms21249561

Yamazaki, J., & Miyoshi, K. (2006). In vitro asymbiotic germination of immature seed and formation of protocorm by Cephalanthera falcata (Orchidaceae). Annals of Botany, 98(6), 1197–1206. https://doi.org/10.1093/aob/mcl223

Yang, F.-S., Sun, A.-H., Zhu, J., Downing, J., Song, X.-Q., & Liu, H. (2017). Impacts of host trees and sowing conditions on germination success and a simple ex situ approach to generate symbiotic seedlings of a rare epiphytic orchid endemic to Hainan Island, China. The Botanical Review, 83, 74–86. DOI: 10.1007/s12229-017-9178-1

Yanoviak, S. P. (2015). Effects of lianas on canopy arthropod community structure. Ecology of Lianas, 343–361. https://doi.org/10.1002/9781118392409.ch24

Yeh, C.-H., Chen, K.-Y., & Lee, Y.-I. (2021). Asymbiotic germination of Vanilla planifolia in relation to the timing of seed collection and seed pretreatments. Botanical Studies, 62(1), 6. https://doi.org/10.1186/s40529-021-00311-y

Yeung, E. C. (2017). A perspective on orchid seed and protocorm development. Botanical Studies, 58(1), 33. https://doi.org/10.1186/s40529-017-0188-4

Yeung, E. C., Li, Y.-Y., & Lee, Y.-I. (2018). Understanding seed and protocorm development in orchids. In: Lee, YI., Yeung, ET. (Eds), Orchid Propagation: From Laboratories to Greenhouses—Methods and Protocols (pp 3–26). New York: Humana Press. https://doi.org/10.1007/978-1-4939-7771-0_1

Yoder, J. A., Zettler, L. W., & Stewart, S. L. (2000). Water requirements of terrestrial and epiphytic orchid seeds and seedlings, and evidence for water uptake by means of mycotrophy. Plant Science, 156(2), 145–150. https://doi.org/10.1016/S0168-9452(00)00246-6

Zarate‐García, A. M., Noguera‐Savelli, E., Andrade‐Canto, S. B., Zavaleta‐Mancera, H. A., Gauthier, A., & Alatorre‐Cobos, F. (2020). Bark water storage capacity influences epiphytic orchid preference for host trees. American Journal of Botany, 107(5), 726–734. https://doi.org/10.1002/ajb2.1470

Zhang, Y., Lee, Y.-I., Deng, L., & Zhao, S. (2013). Asymbiotic germination of immature seeds and the seedling development of Cypripedium macranthos Sw., an endangered lady’s slipper orchid. Scientia Horticulturae, 164, 130–136. https://doi.org/10.1016/j.scienta.2013.08.006

Zhao, D.-K., Selosse, M.-A., Wu, L., Luo, Y., Shao, S.-C., & Ruan, Y.-L. (2021). Orchid reintroduction based on seed germination-promoting mycorrhizal fungi derived from protocorms or seedlings. Frontiers in Plant Science, 12, 701152. https://doi.org/10.3389/fpls.2021.701152

Zotz, G. (2013). The systematic distribution of vascular epiphytes–a critical update. Botanical Journal of the Linnean Society, 171(3), 453–481. https://doi.org/10.1111/boj.12010

Zotz, G., Weigelt, P., Kessler, M., Kreft, H., & Taylor, A. (2021a). EpiList 1.0: a global checklist of vascular epiphytes. Ecology, 102(6), e03326. https://doi.org/10.5167/uzh-202729

Zotz,G., Almeda, F., Arias, S., Hammel, B., & Pansarin, E. (2021b). Do secondary hemiepiphytes exist? Journal of Tropical Ecology, 37(6), 286–290.

Downloads

Additional Files

Published

2025-11-04

How to Cite

Recruitment bottleneck in aphyllous vanilla seedlings facing drought conditions. (2025). Lankesteriana: International Journal on Orchidology, 25(3), 177–199. https://doi.org/10.15517/rwsfdp60