Quantitative Approach for Determining Reproductive Life-History Strategies of Parasitic Plants: A Case Study in Balanophora

摘要

Parasitic plants are a diverse and unique polyphyletic assemblage of flowering plants that survive by obtaining resources via direct vascular connections to a host plant. Ecologically important in their native ecosystems, these typically cryptic plants remain understudied and fundamental knowledge of the biology, ecology, and evolution of most species is lacking. This gap limits our understanding of ecosystems and conservation management. We established a multistep protocol to conduct the first investigation of the reproductive life history of root parasite genus Balanophora, testing the hypotheses of perenniality, cryptic perenniality, and plasticity across five geographically isolated populations in Taiwan. A review of 123 Balanophora publications found contradictory determinations, including no determination (87%), perennial (9%), annual (1%), biennial (1%), or a combination (2%). No primary study investigated the question, and no determination was accompanied by reference. Between 2021 and 2024, we tested a hypothesis of perenniality (109 individuals, 135 patches) and cryptic perenniality (73 host samples), monitored population dynamics (whole population), and potential for endophytic/dormant haustorial tissue (101 roots) across five isolated populations of Balanophora fungosa ssp. fungosa in Taiwan. Our results support semelparous annuality. After reproduction, individuals senesce and die, and the following year's population is recruited from newly germinated individuals which together develop in size and number during a vegetative growth period, undergo reproduction, and then themselves senesce and die. Each cycle is completed within a 12-month period. Synthesis: Our study provides the first quantitative determination of a semelparous annual reproductive life-history strategy for any species of Balanophora. This determination is important in our progress toward better understanding the species—and parasitic plants in general—as well as ecological roles within ecosystems and conservation management. Our study further provides a template for future work to expand life-history strategy determination across cryptic root parasitic plants.

方法與執行步驟

We built a protocol to evaluate the reproductive life history (annual or perennial) of a root parasitic plant and tested it in a case study on Balanophora using a perennial status as our hypothesis. Our protocol was divided into three sections: baseline data (2 steps), hypothesis testing (4 steps), and testing confounding variables (2 steps). We used extensive field studies with large temporal and spatial sampling to characterize the life history of B. fungosa ssp. fungosa in Taiwan.
Baseline Data:Baseline data was used to determine research gap and to locate individuals on which to test hypotheses.Literature Review: We first conducted a comprehensive literature review of all ecological and new species publications on the genus to determine if a reproductive life history had been investigated in any species of Balanophora. Field Surveys: We then conducted comprehensive field surveys, mapping the locations of individuals (which aggregate into ‘patches’) to describe the range of the species within Taiwan (Hengchun Peninsula & Orchid Island).
Hypothesis Testing: Four hypotheses were tested on a representative subset of individuals across five populations (Taiwan Proper n = 3; Orchid Island n = 2), testing a perennial state as our assumed life history. Perennial species will remain healthy after flowering: We tagged and monitored the fate of tubers (n = 109) over two years to measure survival after reproduction. Perennial species will be present all year: We re-surveyed patches in Kenting (35% of total population) and Orchid Island (100%) to determine how many individuals remain between reproductive seasons. Perennial species will have mixed age classes: We conducted bi-weekly surveys of patches (n = 62) over two years to determine size-ratioed age class ranges of individuals in each patch. Perennial species will have stable year-to-year populations: We conducted comprehensive surveys of entire populations at all five sites from 2018-2025 to describe annual population variations.
Confounding Variables: We tested two potential characteristics that may confound hypothesis results, making actual perennial species appear to be annual. Are host species annual: We conducted molecular identification of a representative subset of host trees (n = 88) from all populations. Is the parasitic plant endophytic: We tagged and monitored the infected root section of host trees (n = 51) from 2023-2025 to determine if new tubers commonly arise from the same root locations each year.

創新作為與跨域合作

Determining reproductive life histories of individual species is necessary to properly interpret and analyze ecological and genetic data, and fundamental to conservation. This is particularly important in understudied and often cryptic species such as parasitic plants (ca. 4,750 species globally); we know parasitic plants are important – often keystone – species in their native ecosystems but know very little of their basic biology. Our study was the first to determine the reproductive life history within genus Balanophora : we created a multi-step protocol which we tested in B. fungosa ssp. fungosa (one of six congenerics in Taiwan), providing the first life history designation within the genus. Our results are of importance for the species and parasitic plant biology in general, but more broadly our protocol is a tool researchers can use to expand the breadth (more species) and depth (similar species across different ecosystems) of our understanding of parasitic life histories.

預期成果與貢獻

Our results show that the endangered holoparasitic (obligate) parasitic plant Balanophora fungosa asp. fungosa is in Taiwan an annual species.

Our results first identified a gap in our knowledge of the genus through a comprehensive literature review (n = 123 publications; 1844-2025), finding no previous study had investigated reproductive life histories within genus Balanophora. Our field surveys then identified five unique sites (Taiwan Proper = 3; Orchid Island = 2) with different topographical, climatological, edaphic, and floral characteristics, allowing us to test among-site plasticity.

Our hypothesis testing results found that zero tubers survive after a reproductive event, zero tubers persist in any population between reproductive events, and that each year the entire population is recruited from seed; no multiple-year individuals are found. We also found that populations fluctuated significantly year-to-year but were not consistent among sites. These results were consistent across all sites, over multiple years.

No confounding factors were detected. All identified hosts (n = 88) were perennial trees, and none of the monitored root sections re-grew fresh tubers, suggesting no cryptic perenniality.

Together these results provide a consilience of evidence supporting annuality, and we suggest that this determination holds for the genus across its global range.