Exposure to Water Increased Pollen Longevity of Pondweed

Evol Ecol (2010) 24:939–953 DOI 10.1007/s10682-010-9351-z ORIGINAL PAPER Exposure to water increased pollen longevity of pondweed (Potamogeton spp.) indicates different mechanisms ensuring pollination success of angiosperms in aquatic habitat Xiao-lin Zhang • Robert W. Gituru • Chun-feng Yang • You-hao Guo Received: 8 December 2008 / Accepted: 4 January 2010 / Published online: 22 January 2010 Ó Springer Science+Business Media B.V. 2010 Abstract Pollen longevity in seven Potamogeton species representing different pollination systems (anemophily, epihydrophily and hydroautogamy) was assessed both under aerial condition and in contact with water to investigate how water impacts the sexual reproduction in these aquatic taxa. Stainability of pollen with MTT was considered as an indicator of pollen viability. The half-life of pollen longevity was calculated using exponential decay regression. Overall, pollen viability decreased relatively rapidly with time. Pollen grains of obligate anemophilic species had lower initial viability and shorter half- lives than those of facultative anemophilic species. Pollen in these latter species may take more time to reach the stigma. The pollen of Potamogeton may be categorized as partially hydrated pollen owing to its generally spherical shape and lack of furrows, rapid loss of viability, and fast pollen tube initiation. The half-life is positively correlated with pollen size. Smaller-sized grains are at greater risk of desiccation than larger grains. In contrast with the situation observed in most terrestrial angiosperms, contact with water increases pollen longevity in Potamogeton species. In our present study the half-lives of pollen longevity of Potamogeton species in which the pollen had come into contact with water (mean of 10.65 h) were markedly higher than those under aerial conditions (mean of 5.79 h, t = 2.622, P = 0.039). The results of our study contradict a widely held belief that water is detrimental to pollen viability in angiosperms and furthermore indicate that close X. Zhang Á C. Yang (&) Á Y. Guo (&) College of Life Sciences, Wuhan University, 430072 Wuhan, China e-mail: [email protected] Y. Guo e-mail: [email protected] X. Zhang Institute of Hydrobiology, Chinese Academy of Sciences, 430072 Wuhan, China R. W. Gituru Botany Department, Jomo Kenyatta University of Agriculture and Technology, 62000-00200 Nairobi, Kenya C. Yang Wuhan Botanical Garden, Chinese Academy of Sciences, 430074 Wuhan, China 123 940 Evol Ecol (2010) 24:939–953 proximity to water results in selection for wettability. The transition to a hydrated status together with its morphology, make Potamogeton pollen more adapted to the aquatic environment and thus serves to ensure reproductive process. Results of our present study may have direct implications for understanding the evolution of the sexual reproductive system in aquatic angiosperms. Keywords Pollen longevity Á Half-life Á Selective pressure Á Pondweed Á Potamogeton Introduction Pollen loss during pollination process is a common phenomenon but the intensity of the loss is different in taxa with different pollination systems (Harder and Thomson 1989). Pollen loss is also considered to occur when a proportion of the pollen grains lose their male function e.g., when pollen grains lose viability before deposition on the stigma. Pollen viability is generally considered to indicate the ability of the pollen grain to perform its function following compatible pollination (Shivanna et al. 1991), and pollen longevity has been considered as an important ecological and evolutionary character of angiosperms (Dafni and Firmage 2000). Pollen viability commonly declines after release from the anthers. The term half-life is widely used in research because the data are easy to understand and they lend themselves easily to comparisons (Bryan et al. 1990). In addition, half-life provides a useful summary statistic for a population. However, only a few studies have attempted to quantify the analysis of pollen longevity (Khatun and Flowers 1995; Castellanos et al. 2006; Song et al. 2001). Many factors including humidity, temperature and the vagaries of the weather may reduce pollen viability and longevity (Bassani et al. 1994; Hedhly et al. 2005; Boavida and McCormick 2007; Song and Tachibana 2007). It has been demonstrated that contact with water and high levels of humidity markedly reduce pollen longevity in many terrestrial angiosperms (Gilissen 1977; Shivanna and Heslop-Harrison 1981; Huang et al. 2002; Mao and Huang 2009). Consequently, plants have evolved different mechanisms to avoid water related reduction in pollen longevity (Bynum and Smith 2001; Huang et al. 2002; Mao and Huang 2009) and ensure the accomplishment of male function even under unfavorable environments. Most aquatic angiosperms are thought to have evolved from their terrestrial ancestors on many independent occasions (Philbrick and Anderson 1987; Cook 1988, 1990; Philbrick and Les 1996) and hydrophily is considered to have been derived from anemophily (Arber 1920; Daumann 1963; Sculthorpe 1967; Philbrick 1988). In aquatic habitats, the pollination process is highly likely to be affected by the presence of water. Water must be an important source of selective pressure in the evolution of the pollination systems in plants living in these habitats. Considering that the preservation of pollen viability is of critical importance during the pollination process, it is crucial to investigate the response of the pollen of aquatic plants to contact with water in comparison to the pollen of terrestrial species. Such investigations may provide useful insights into the adaptation to aquatic environment instead of terrestrial environment of aquatic angiosperms since they are thought as a group derived from terrestrial ancestors. Potamogeton Linn. (Pondweed) is the largest angiosperm genus consisting entirely of aquatic species. Extensive morphological diversity and different pollination types have been found in this genus. This diversity is considered to have resulted from the intense selective 123 Evol Ecol (2010) 24:939–953 941 pressure in the aquatic habitat (Zhang et al. 2009). Although anemophily (wind pollination) is the main pollination type in this genus (Sculthorpe 1967; Cook 1988), epihydrophily (pollen grains are transported on water surface by water currents to the floating inflorescences) and hydroautogamy (self-pollination is achieved with the aid of bubbles when anthers dehisce Philbrick 1988; Guo and Cook 1990), also play a considerable role. Natural pollen transfer in almost all species of Potamogeton, may occur under two conditions: namely aerial condition and water condition. Under the aerial condition, pollen grains are transported entirely by air currents and they do not come into contact with water. In the water, pollen grains are transported by water currents or bubbles to the floating receptive inflorescences. Both of these two conditions of pollen transfer may occur in Potamogeton. Consequently, the pollen grains in these plants are likely to come into contact with water. There may exist a different pattern of pollen performance in aquatic plants com- pared to terrestrial angiosperms. It is therefore interesting to study how exposure to water affects the pollen grains in this genus. Our present study focused on the response of the pollen grains of Potamogeton under aerial and water conditions. Using information obtained partly from monitoring pollen viability under these two conditions and from calculation of the half-life of pollen longevity using the exponential decay regression, we proposed the likely mechanisms by which the pollen of Potamogeton maintains viability even after contact with water. The importance of hydration of pollen for Potamogeton species and its evolutionary implications are discussed. We also discuss the correlations among pollen traits, pollination types, and floral traits in Potamogeton. Materials and methods Study species Potamogeton Linn., with more than 100 species, is the largest genus of flowering plants in which all members are aquatic in habitat. The genus has a worldwide distribution but is concentrated in the Northern Hemisphere (Wiegleb and Kaplan 1998). Species in this genus display a range of morphological variation and habitat. Consequently three main pollination types are found in the genus namely anemophily, epihydrophily and hydroautogamy (Philbrick 1988; Zhang et al. 2009). For the present study we selected seven representative species representing all pollination types in the genus to investigate the effect of contact with water on pollen longevity. The experiments were performed during the summer of 2007 and 2008. Pollen was col- lected from several natural populations, and voucher specimens were preserved in Wuhan University Herbarium (WH), P. R. China. We also recorded the natural pollination process in these species and their overall morphology. Much of the detailed floral characteristics in our study populations, except for the natural seed set of the P. malaianus population which is located in Shanxi province, had been documented in an earlier study (Zhang et al. 2009). Pollen longevity under different conditions Pollen stainability is commonly used as an indicator of pollen viability (Dafni and Firmage 2000). In the present study we considered stainability of pollen with 2,5-diphenyl tetrazolium bromide (MTT) as an indication of pollen viability. MTT is a vital dye that detects the presence of dehydrogenase in viable pollen (Khatun

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