A global review of watermelon pollination biology and ecology: The increasing importance of seedless cultivars

Highlights

• Watermelon is the most commonly grown cucurbit in the world that entirely depends on insect pollinators.

• Watermelon cultivars include those that are seeded (i.e. diploid) and hybrid seedless (i.e. triploid).

• Seedless watermelon requires pollen grains to be moved from seeded cultivars because their own pollen is not viable.

• Pollination is likely to be more challenging for seedless cultivars of watermelon than it is for seeded cultivars.

• Pollination requirements and pollinator effectiveness across genotypes and growing regions require research attention.

Abstract

Many commercially grown fruits and vegetables benefit substantially from biotic pollination, worth more than US$ 316 bn to the global economy. Watermelon is one of the most economically important global food crops both in terms of production quantity (118.4 million tons (MT)) and production value (GDP US$ 33.9 million). Here, we review the current state of knowledge on the pollination ecology of seeded and seedless watermelons. Specifically we compare the floral biology, pollination requirements and production. Triploid watermelon cultivars (seedless) are becoming more widespread compared to traditional diploids (seeded). However, few published studies have focused on seedless cultivars due to their relatively recent cultivation. The results of this review indicate that different watermelon genotypes require specific management to ensure optimal production.

Introduction

Animal-mediated pollination is an ecosystem service that enhances the quantity and quality of horticultural food production. Yet, new cultivars are being developed and growing regions are rapidly expanding and we know surprisingly little about the pollination ecology and biology of many recent cultivars and hybrids. Watermelon (Citrullus lanatus [Thunb.] Matsum and Nakai; family: Cucurbitaceae) is the most commonly grown cucurbit in the world that entirely depends on insect pollinators due to its monecious flowering habit and large sticky pollen grains (Free, 1993; McGregor, 1976; Delaplane and Mayer, 2005). This annual creeping herb native to Southern Africa (Free, 1993) has become one of the most economically important global food crops, both in terms of production quantity (118.4 million MT in 2017) and production value (GDP US$ 33.9 million in 2016) (FAO, 2017). Watermelon is now grown in 122 countries and around 1,200 cultivars are grown on all cultivated continents (Tibor, 1993; Adeoye et al., 2011). China currently produces the largest quantity, followed by Iran, Turkey and Brazil (FAO, 2017). Watermelon fruit produced from numerous cultivars differ in size (ice box, small, medium and gigantic), shape (round, oval, blocky or elongate) and flesh colour (white, orange, green or red), in accordance with consumer preferences (Kyriacou et al., 2018).

Watermelon cultivars include those that are seeded (i.e. diploid) and hybrid seedless (i.e. triploid). Hybrids (a genetic "cross" between two organisms of different breeds, varieties, species or genera) of most crops often display increased yield, enhanced yield stability, and improved abiotic and biotic stress resistance (Schnable and Springer, 2013). The concept of hybrid seedless watermelon was described first in Kihara (1951) based on an experiment conducted in Japan but widespread cultivation started in the 1990′s. Seedless watermelons have become more popular and widely available throughout the world due to the lack of seeds, consumer preference and the greater economic value to growers over traditional seeded cultivars (Marr and Gast, 1991; Gunter et al., 2007). For example, in the USA alone over 80% of grown watermelons are seedless and the price of seedless watermelon varies between US$ 0.46−0.55 per pound, while the price of seeded watermelon is lower, varying between US$ 0.31−0.38 (AgMRC, 2018).

Despite lacking seeds, pollination is still required in seedless cultivars as fruit set and quality is reliant on growth hormones released by pollen tube growth and ovule fertilization (Gillaspy et al., 1993). Critically, seedless watermelon pollination requires pollen grains to be moved from seeded cultivars (i.e. pollen donors) because their own pollen is not viable (Maynard and Elmstrom, 1989; Fiacchino and Walters, 2003; Freeman et al., 2007a). Male flowers of triploid cultivars thus have a limited contribution to pollen availability and pollination. In contrast, in diploid cultivars, pollen grains of male flowers are largely viable and available for pollen removal and transfer. The presence of diploid flowers results in more male flowers available per plant within a given area and will likely mean a greater probability of pollen transfer via pollinator visits. For these reasons, pollination of seedless cultivars requires additional planning and has potential to be more challenging than pollination in seeded cultivars. However, due to their relatively recent cultivation, few published studies have focused on seedless cultivars. As a result, there is currently a lack of information on the pollination requirements of seedless cultivars and how these requirements differ from seeded cultivars.

Here, we compare the floral biology, pollination, and production requirements of both seeded and seedless watermelon. Further, we identify the current knowledge gaps that may guide future research to enhance the pollination efficacy and productivity of seedless watermelon.