Mixed mating system and intraspecific variation in lizard pollination of Withania frutescens (L.) Pauquy.

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.