Implications of seed germination ecology for conservation of Camptotheca acuminata, a rare, endemic, and endangered species in China

Abstract

Seed germination and seedling recruitment are among the most critical stages for plant population persistence and development, which may be influenced by habitat fragmentation and resulting microhabitat changes. We conducted laboratory and field experiments using seeds of Camptotheca acuminata, a rare, endemic, and endangered species in China, to investigate the effects of temperature change and water availability on seed viability and germination. The seeds were sensitive to high temperature and water stress. Germination percentages > 60% occurred only between 20–35 °C and water potentials >  − 0.6 MPa. Heating at 75 °C and above for 30 min, continuous heating at 40 °C for 20 days, or desiccation following 120 h imbibition killed nearly all seeds. These seed traits made none of the five microhabitats investigated suitable for regeneration. In the understory plot, most seeds germinated, but the resultant seedlings survived only a short time, depending on reserve food supply from the seeds. Sensitivity to high temperature and water stress inhibited germination in the other plots and most seeds died in the hydration-dehydration cycles. We concluded that efficient natural regeneration could occur only in very special habitats: cool, with stable moist soil but ample sunlight, most likely in suitable gaps in continuous forests. In addition to habitat loss and over-exploitation, difficulties in natural seed germination and seedling recruitment are primary reasons for the current status of C. acuminata. For population recovery of C. acuminata, understory microhabitat protection and artificial support for germination and seedling recruitment are required.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Data availability

All data were presented in this manuscript.

References

  1. Ashworth L, Martí ML (2011) Forest fragmentation and seed germination of native species from the Chaco serrano forest. Biotropica 43:496–503

    Article  Google Scholar 

  2. Bruna EM (2002) Effects of forest fragmentation on Heliconia acuminata seedling recruitment in Central Amazonia. Oecologia 132:235–243

    Article  Google Scholar 

  3. Butler LH, Hay FR, Ellis RH, Smith RD, Murray TB (2009) Priming and re-drying improve the survival of mature seeds of Digitalis purpurea during storage. Ann Bot 103:1261–1270

    CAS  Article  Google Scholar 

  4. Cascante A, Quesada M, Lobo J, Fuchs EA (2002) Effects of dry tropical forest fragmentation on the reproductive success and genetic structure of the tree Samanea saman. Conserv Biol 16:137–147

    Article  Google Scholar 

  5. Chen SY, Zhang XZ (2018) Characterization of the complete chloroplast genome of the relict Chinese false tupelo, Camptotheca acuminate. Conserv Genet Resour 10:659–662

    Article  Google Scholar 

  6. Dalling JW, Davis AS, Schutte BJ, Arnold AE (2011) Seed survival in soil: interacting effects of predation, dormancy and the soil microbial community. J Ecol 99:89–95

    Article  Google Scholar 

  7. Daws MI, Bolton S, Burslem DFP, Garwood NC, Mullins CE (2007) Loss of desiccation tolerance during germination in neo-tropical pioneer seeds: implications for seed mortality and germination characteristics. Seed Sci Res 17:273–281

    Article  Google Scholar 

  8. Donohue K, Rubio de Casas R, Burghardt L, Kovach K, Willis CG (2010) Germination, postgermination adaptation, and species ecological ranges. Annu Rev Ecol Evol Syst 41:293–319

    Article  Google Scholar 

  9. Gascon C, Williamson GB, da Fonseca GAB (2000) Receding forest edges and vanishing reserves. Science 288:1356–1358

    CAS  Article  Google Scholar 

  10. Gonzalez-Zertuche L, Vazquez-Yanes C, Sánchez-Coronado GA et al (2001) Natural priming of Wigandia urens seeds during burial: effects on germination, growth and protein expression. Seed Sci Res 11:27–34

    CAS  Article  Google Scholar 

  11. Griffith AB, Forseth IN (2005) Population matrix models of Aeschynomene virginica, a rare annual plant: implications for conservation. Ecol Appl 15:222–233

    Article  Google Scholar 

  12. Hao JH, Lv SS, Bhattacharya S, Fu JG (2017) Germination response of four alien congeneric Amaranthus species to environmental factors. PLoS ONE 12:e0170297. https://doi.org/10.1371/journal.pone.0170297

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  13. Herranz JM, Ferrandis P, Martínez-Duro E (2010) Seed germination ecology of the threatened endemic Iberian Delphinium fissum subsp.sordidum (Ranunculaceae). Plant Ecol 211:89–106

    Article  Google Scholar 

  14. Honěk A, Martinková Z (1996) Geographic variation in seed dormancy among populations of Echinochloa crus-galli. Oecologia 108:419–423

    Article  Google Scholar 

  15. Jordi LP, Zhao AM (2004) China: a rich flora needed of urgent conservation. Orsis 19:49–89

    Google Scholar 

  16. Lamont BB, Van Leeuwen SJ (1988) Seed production and mortality in a rare Banksia species. J Appl Ecol 25:551–559

    Article  Google Scholar 

  17. Lang ARG (1967) Osmotic coefficients and water potentials of sodium chloride solutions from 0 to 40 °C. Aust J Chem 20:2017–2023

    CAS  Article  Google Scholar 

  18. Li HM, Ma YX, Liu WJ, Liu WJ (2009) Clearance and fragmentation of tropical rain forest in Xishuangbanna, SW, China. Biodivers Conserv 18:3421–3440

    Article  Google Scholar 

  19. Liu JJ, Slik JWF (2014) Forest fragment spatial distribution matters for tropical tree conservation. Biol Conserv 171:99–106

    Article  Google Scholar 

  20. Liu JM (1998) The dormancy of the seed and the regeneration of Camptotheca acuminate. J Southw China Norm Univ (Nat Sci Ed) 23:721–725 ((in Chinese with English abstract))

    Google Scholar 

  21. Long RL, Gorecki MJ, Renton M, Scott JK, Colville L et al (2015) The ecophysiology of seed persistence: a mechanistic view of the journey to germination or demise. Biol Rev 90:31–59

    Article  Google Scholar 

  22. Long RL, Kranner I, Panetta FD, Birtic S, Adkins SW, Steadman KJ (2011) Wet-dry cycling extends seed persistence by re-instating antioxidant capacity. Plant Soil 338:511–519

    CAS  Article  Google Scholar 

  23. Ma YX, Liu YH, Zhang KY (1998) On microclimate edge effects of tropical rainforest fragments in Xishuangbanna. Acta Phytoecol Sin 22:250–255 ((in Chinese with English abstract))

    Google Scholar 

  24. Matthies D, Bräuer I, Maibom W, Tscharntke T (2004) Population size and the risk of local extinction: empirical evidence from rare plants. Oikos 105:481–488

    Article  Google Scholar 

  25. Michel BE (1983) Evaluation of water potentials of solutions of polyethylene glycol 8000 both in the absence and presence of other solutes. Plant Physiol 72:66–70

    CAS  Article  Google Scholar 

  26. National Forestry Bureau and Agriculture Ministry of China (1999) List of national key protected wild plants (first group). National Forestry Bureau and Agriculture Ministry of China, Beijing, China

    Google Scholar 

  27. Ren H, Zhang QM, Lu HF, Liu HX, Guo QF, Wang J, Jian SG, Bao HO (2012) Wild plant species with extremely small populations require conservation and reintroduction in China. Ambio 41:913–917

    Article  Google Scholar 

  28. Vergeer P, Rengelink R, Copal A, Ouborg NJ (2003) The interacting effects of genetic variation, habitat quality and population size on performance of Succisa pratensis. J Ecol 91:18–26

    CAS  Article  Google Scholar 

  29. Ward M, Johnson SD (2005) Pollen limitation and demographic structure in small fragmented populations of Brunsvigia radulosa (Amaryllidaceae). Oikos 108:253–262

    Article  Google Scholar 

  30. Wen B (2019) Seed germination ecology of Alexandra palm (Archontophoenix alexandrae) and its implication on invasiveness. Sci Rep 9:4057

    Article  Google Scholar 

  31. Wen B (2015) Effects of high temperature and water stress on seed germination of the invasive species Mexican sunflower. PLoS ONE 10:e0141567. https://doi.org/10.1371/journal.pone.0141567

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  32. Wen B, Liu MH, Tan YH, Liu Q (2016) Sensitivity to high temperature and water stress in recalcitrant Baccaurea ramiflora seeds. J Plant Res 129:637–645

    CAS  Article  Google Scholar 

  33. Wen B, Xue P, Zhang N, Yan Q, Ji MY (2015) Seed germination of invasive species Piper aduncum as affected by high temperature and water stress. Weed Res 55:155–162

    Article  Google Scholar 

  34. Ye J, Wen B (2017) Seed germination in relation to the invasiveness in spiny amaranth and edible amaranth in Xishuangbanna, SW, China. PLoS ONE 12:e0175948

    Article  Google Scholar 

  35. Zhang Z, Li S, Zhang S, Liang C, Gorenstein D, Beasley RS (2004) New camptothecin and ellagic acid analogues from the root bark of Camptotheca acuminata. Planta Med 70:1216–1221

    CAS  Article  Google Scholar 

  36. Zhou YS (1989) Dormancy and germination characteristics in Camptotheca acuminate seeds. For Appl Technol 1989:22–25 ((in Chinese))

    Google Scholar 

  37. Zhu H, Wang H, Zhou SS (2010) Species diversity, floristic composition and physiognomy changes in a rainforest remnant in Southern Yunnan, China after 48 years. J Trop For Sci 22:49–66

    Google Scholar 

  38. Zhu H, Xu ZF, Wang H, Li BG (2004) Tropical rain forest fragmentation and its ecological and species diversity changes in southern Yunnan. Biodivers Conserv 13:1355–1372

    Article  Google Scholar 

Download references

Acknowledgements

We are grateful to the National Natural Science Foundation of China (31971573) for providing financial support for this research, and Prof Richard T. Corlett is thanked for kindly reviewing this manuscript.

Funding

We are grateful to the National Natural Science Foundation of China (31971573) for providing financial support for this research.

Author information

Affiliations

Authors

Contributions

BW: Conceptualization, Methodology, Investigation, Formal analysis, Supervision, Funding acquisition, Writing—review & editing; PY: Investigation, Formal analysis, Review & editing.

Corresponding author

Correspondence to Bin Wen.

Ethics declarations

Conflict of interest

The authors declare no conflicts of interest.

Consent to participate

Both listed authors have agreed to participate.

Consent for publication

Both listed authors have approved the manuscript before submission, including the names and order of authors.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Communicated by Thomas Abeli.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Wen, B., Yang, P. Implications of seed germination ecology for conservation of Camptotheca acuminata, a rare, endemic, and endangered species in China. Plant Ecol (2020). https://doi.org/10.1007/s11258-020-01099-w

Download citation

Keywords

  • Habitat fragmentation
  • High-temperature tolerance
  • Medicinal tree
  • Plant diversity conservation
  • Water stress