Abstract
Though some hypotheses have obtained theoretical and empirical supports, it remains largely unknown in the aspect that how deception increases orchid fitness. This study used food-deceptivePapilionanthe teres as experimental material to explore the ecological significance of orchid deceptive pollination. Deception together with obvious pollinarium bending increases P. teres fitness by means of decreasing geitonogamy under the natural conditions. The proportions of full seeds, single fruit weight and seed weight per fruit after self-pollination and nectar addition were significantly lower than that after cross-pollination and natural conditions (all p < 0.05). Seed viability (seed growth and development rate) after cross-pollination and natural condition were significantly higher than that after self-pollination and nectar addition (all p < 0.05). However, there was no significant difference in all the above parameter values of fruits and seeds between cross-pollination and natural conditions (all p > 0.05). These results confirmed that P. tereshas high level of genetic load, and self-fertilization or geitonogamy will cause serious inbreeding depression. These conclusions support the outcrossing hypothesis that ecological significance of P. teresdeception is to promote outcrossing and improve the ability of the offspring to adapt to the environment.
Keywords: Papilionanthe teres, deception, geitonogamy, inbreeding depression, outcrossing
Introduction
Orchidaceae is a large family of plants, with about 763 genera and 28000 species (Crain & Tremblay, 2014; Christenhusz & Byng, 2016; Zhang et al., 2018). Of the 7500 angiosperm species that are pollinated through deception, approximately 6500 are orchids (Renner, 2006), suggesting that deception mainly occurs in orchids. Food deception is most prevalent in the orchid family, and several thousand species are found in 38 genera (Dafni, 1984; Ackerman, 1986; Nilsson 1992; Jersáková et al., 2006). The second is sexual deception, and about 400 orchid species are found in 18 genera (Dafni & Bernhardt, 1990; Cozzolino & Widmer, 2006; Jersáková et al., 2006).
Visit frequency and natural fruit set of no rewarding species are lower than that of rewarding ones due to pollinator learning behavior. So the fitness of deceptive plants remains a focus for debate among biologists. Besides four orchid-specific hypotheses (Jersáková et al., 2006; Cozzolino & Widmer, 2006; Scopece et al., 2010), there are two general hypotheses, resource-limitation hypothesis and outcrossing hypothesis, to explain how deception increases plant fitness (Jersáková et al., 2006).
Plant sexual reproduction, such as flower production and fruit set, is mainly limited by resources (Calvo, 1992; Mattila & Kuitunen, 2000). The aim of deception is to invest more resources to maintain plant development and ensure a certain seed set (resource-limitation hypothesis) (Ackerman & Montalvo, 1990; Barrett & Harder, 1995). However, the sexual reproduction of deceptive orchids is often severely limited by pollens over a lifetime (Calvo, 1993; Tremblay et al., 2005). Hence, it is difficult to understand why resources in these orchids are not allocated to a component of pollinator attraction such as nectar. One possibility is that the attraction of investing more resources in floral display is more efficient than that in rewarding substances.
Deception results in lower visitation rates, fewer flowers probed per visit, lower level of geitonogamy, more pollen output and outcrossed progeny (outcrossing hypothesis) (Jersáková et al., 2006). Based on the above conclusions, it is widely believed that loss of rewarding substances contributes to decreasing geitonogamy and promoting outcrossing (Dressler, 1981; Nilsson, 1992; Johnson & Nilsson, 1999). Outcrossing hypothesis emphasizes the importance of pollen resource and genetic quality in reproductive success, and postulates that self-fertilization or geitonogamy will cause inbreeding depression (Lammi & Kuitunen, 1995). Therefore, the first problem of outcrossing hypothesis is to test whether self and cross-pollination result in different female reproductive success (Lammi & Kuitunen, 1995). Though previous case studies confirm that deception promotes outcrossing, whether actual outcrossing rates are generally higher in deceptive orchids remains unknown (Jersáková et al., 2006).
Pollinarium bending occurres in many orchid species, it will result in a time delay before the pollinium assumes a position from which it can strike a stigma (Darwin, 1877; Johnson & Edwards, 2000). The phenomenon will decrease geitonogamy when pollinators visit fewer flowers and stay for shorter time per visit. Some case studies confirm that pollinarium bending is an anti-selfing mechanism (Darwin, 1877; Johnson et al., 2004). These results suggest that pollinarium bending may increase orchid fitness under certain conditions. But it still requires further study that how pollinarium bending increases fitness in orchid deceptive pollination systems.
Papilionanthe teres is only found in a very limited region of southeast Xishuangbanna in China. It has adapted to high temperature, humidity and sunlight conditions. Its flowers exhibit color polymorphism of the corolla, such as white lateral sepal, purplish red petal, dorsal sepal and labellum (Zhou & Gao, 2016). Its single inflorescence may bear 1-16 flowers. Floral longevity may reach more than 30 days under the conditions of no pollinarium removal, pollinia deposition and floral damage. P. teres is a typical food-deceptive species, with no reward in its flowers. The techniques of symbiotic and asymbiotic seed reproduction in P. teres were established in previous studies (Chen et al., 2007; Mazumder et al., 2010; Zhou & Gao, 2016; Vishal, 2020). This study utilized these techniques and used P. teres as material to understand the ecological significance of orchid deceptive pollination. The following questions were addressed: (1) What are the mechanisms of promoting outcrossing in P. teres ? (2) What are the effects of self-pollination and nectar addition on fruit and seed development and seed viability of P. teres ? (3) Does self and cross pollination result in different female reproductive success? (4) Does P. teres have a high outcrossing rate (high levels of genetic load) under natural conditions?
Material and Methods