Mixed mating system and intraspecific variation in lizard pollination of Withania frutescens (L.) Pauquy – PubMed Black Hawk Supplements
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Plant reproductive strategies are particularly relevant on islands, where environmental constraints usually shape ecological dynamics. In this sense, the role of lizards (Lacertilia) as flower visitors and potential pollinators has been increasingly recognized. However, lizards may also consume plant reproductive tissues, potentially influenced by lizard intraspecific traits such as age and sex. This study aims to investigate, for the first time, the reproductive biology of the rare…
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Mixed mating system and intraspecific variation in lizard pollination of Withania frutescens (L.) Pauquy
Raquel Muñoz-Gallego et al. AoB Plants. .
Abstract
Plant reproductive strategies are particularly relevant on islands, where environmental constraints usually shape ecological dynamics. In this sense, the role of lizards (Lacertilia) as flower visitors and potential pollinators has been increasingly recognized. However, lizards may also consume plant reproductive tissues, potentially influenced by lizard intraspecific traits such as age and sex. This study aims to investigate, for the first time, the reproductive biology of the rare Mediterranean shrub Withania frutescens (L.) Pauquy (Solanaceae), and to assess the role of the Balearic lizard Podarcis lilfordi Günther (Lacertidae) as a potential pollinator on Na Redona islet (Cabrera archipelago, Balearic Islands). We analysed flower traits (corolla length, corolla diameter, stamen length, and pistil length) and performed flower bagging experiments with three pollination treatments (open pollination, autogamy, and cross hand-pollination) from 2018 to 2021 to unravel the plant reproductive system. Fruit set, the number of seeds per fruit, seed weight, size and viability were then assessed. Observational censuses were conducted to identify the main flower visitors and estimate their visitation frequency. Finally, we measured morphometric traits of lizards and explored potential intraspecific variation in floral use. The flowers of W. frutescens were morphologically hermaphroditic but functionally dioecious, spatially separated in unisexual individual plants. Open pollination and autogamy treatments resulted in similar fruit set, while cross hand-pollination produced the highest value. However, open pollination significantly increased seed weight and viability. Lizards were the most frequent floral visitors, accounting for 68% of visits, while insects made up the remaining 32%. Lizards played a dual role as both pollinators and florivores, with 45% of their visits potentially contributing to pollination and 55% involving florivory. Juveniles and females primarily conducted legitimate visits, whereas males -with a larger size- were more likely to consume the flowers. Our research describes, for the first time, a mixed reproductive system in W. frutescens, combining hermaphroditism with cryptic dioecy. We also provide a new example of a lizard-pollinated plant, highlighting the importance of vertebrates on island pollination as well as the influence of pollinator intraspecific variation on plant reproductive success. Further research on the reproductive and pollination systems of small, isolated plant populations is crucial, given their heightened vulnerability to disturbance and genetic inbreeding.
Keywords: Podarcis lilfordi; autogamy; cryptic dioecy; double mutualism; florivory; functional dioecy; islands; reproductive system.
© The Author(s) 2025. Published by Oxford University Press on behalf of the Annals of Botany Company.
Figures

(A) Large individual of W. frutescens located in a cliff of Na Redona (Cabrera Archipelago National Park, Balearic Islands). (B) Bell-shaped flower of W. frutescens. (C) Ripening fruits of W. frutescens.

(A) Functional female plant of W. frutescens, bearing typical flowers with a longer functional pistil and shorter sterile anthers (brown structure located behind the calyx in the image), as well as fruits. (B) Functional male plant of W. frutescens, bearing typical flowers with functional anthers of similar length to the sterile pistil. Bar represents scale (1 mm) of the magnifying glass photographs. (C) Corolla length, corolla diameter, stamen length and pistil length (mm) by flower morph: female (n = 146 for all traits, except pistil length where n = 145) or male (n = 114). Asterisks denote statistical significance: *** P < 0.001.

Fruit set (number of fruits/number of bagged flowers; n = 10 plants per treatment), seed weight (mg), seed width (mm) and seed viability (proportion of TTZ positives; n = 57, 42, and 57 seeds for open pollination, autogamy, and cross hand-pollination treatments, respectively) depending on the pollination treatment for female plants. Note that fruit set for male plants was zero. Bars represent adjusted means ± standard error from post-hoc Tukey test. Different letters denote significant differences between paired levels in post-hoc comparisons.

(A) Individual of P. lilfordi legitimaly visiting a flower of Withania frutescens flower. (B) Mean probability of florivory on W. frutescens flowers depending on the lizard group: juveniles (n = 15), females (n = 9), and males (n = 16). Points represent the mean probability, lines the upper and lower standard errors, and different letters denote significant differences between paired levels in post-hoc comparisons. (C) Gape width (mm) of P. lilfordi depending on the lizard group (female, n = 18; male, n = 17). Asterisks denote statistically significant differences: *** P < 0.001.
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