Plant Syst Evol (2010) 286:191–197 Author's personal copy DOI 10.1007/s00606-010-0299-9 ORIGINAL ARTICLE Pollen and ovule production in wind-pollinated species with special reference to Juncus Stefan G. Michalski • Walter Durka Received: 13 August 2009 / Accepted: 21 April 2010 / Published online: 19 May 2010 Ó Springer-Verlag 2010 Abstract The reproductive biology of wind-pollinated species. We argue that woody perennials, independent of species in terms of pollen and ovule production is rarely dicliny, may be preferentially outcrossed and therefore studied compared with zoophilous species, despite avail- exhibit decreased variation in mating systems compared able hypotheses on the effect of growth form and life- with herbs. Because the degree of outcrossing correlates history traits on reproductive investment. Here, we use with P/O ratios, differences between homoecious published data and new data for species of Juncus and and nonhomoecious woody perennials could be less Luzula (Juncaceae) to test the hypotheses that, in wind- pronounced. pollinated species, woody perennials should exhibit larger pollen–ovule (P/O) ratios than herbaceous species and that Keywords Juncus Á Juncaceae Á Wind pollination Á species with separate sexes have larger P/O ratios than Pollen–ovule ratios Á Mating system Á Life history homoecious species. In total, we report pollen and ovule production for 291 wind-pollinated species, including 19 Juncus and 5 Luzula species. Compared with other wind- Introduction pollinated species, Juncus exhibits unusually low P/O ratios (log P/O = 2.06 ± 0.46) because of high ovule Wind pollination is known from at least 18% of all production. We argue that the high ovule and seed pro- angiosperm families (Ackerman 2000) and has evolved duction in Juncus, associated with frequent self-fertiliza- repeatedly from biotically pollinated ancestors (Linder tion, may be beneficial in habitats preferred by the genus. 1998). On the level of regions or communities, it is more In general, we found higher P/O ratios in woody perennials common in higher latitudes and altitudes, in temperate (log P/O = 4.37 ± 1.18) or in species with separate sexes forests and open grasslands (Regal 1982; Whitehead 1983). (log P/O = 4.28 ± 1.12) than in herbaceous (log P/O = Certain climatic and ecological factors may favor the 3.51 ± 0.77) or homoecious (log P/O = 3.52 ± 0.80) occurrence and evolution of anemophily, such as dry species, respectively. However, when we analyzed woody conditions, open vegetation, uncertainty of pollinators, and perennials separately, we found no significant difference in high density of conspecifics (Whitehead 1969; Stebbins P/O ratios between homoecious and nonhomoecious 1970; Niklas 1985; Ackerman 2000; Culley et al. 2002). In contrast to the floral variability found in zoophilous taxa, anemophily seems to be evolutionarily connected to very Electronic supplementary material The online version of this similar morphological adaptations (Pohl 1929; Whitehead article (doi:10.1007/s00606-010-0299-9) contains supplementary 1969; Friedman and Barrett 2008). Consequently, a number material, which is available to authorized users. of traits associated with wind pollination constitute the S. G. Michalski (&) Á W. Durka anemophilous syndrome (Faegri and Van Der Pijl 1979; Helmholtz Centre for Environmental Research UFZ, Ackerman 2000). For example, inflorescences of wind- Department of Community Ecology (BZF), pollinated species are often condensed and catkin-like, and Theodor-Lieser-Strasse 4, 06120 Halle, Germany their nectarless flowers are often unisexual with an absent e-mail: [email protected] or reduced perianth (Culley et al. 2002; Friedman and 123 192 Author's personal copy S. G. Michalski, W. Durka Barrett 2008). However, some wind-pollinated and evolu- species could be evaluated with more explanatory power. tionarily very successful groups such as Poaceae and In general, life form and pollination mode have been Juncaceae exhibit hermaphroditic flowers, challenging the found to contribute significantly to variation in P/O hypothesis of an association between unisexuality and wind ratios (Michalski and Durka 2009). However, because pollination (Charlesworth 1993). woody perennials might be, on average, larger than Floral adaptation to anemophily is believed to include herbaceous plants, it was hypothesized that, especially in modifications of ovule and pollen production per flower. wind-pollinated species, several size effects could lead to For example, in wind-pollinated flowers, ovule number is increased floral male allocation, and thus higher P/O frequently reduced to one (Pohl 1929; Friedman and ratios, in woody perennials than in herbaceous plants Barrett 2008), and several non-mutually exclusive expla- (Michalski and Durka 2009). Also, Cruden (2000) nations for this fact have been proposed. First, capturing hypothesized that, in wind-pollinated species with only sufficient pollen grains to fertilize many ovules is unlikely homoecious, hermaphroditic flowers, P/O ratios were in a stochastic process such as wind pollination. Second, lower than in species with a monoecious or dioecious uniovulate carpels may increase male–male competition. sexual system. He argued that, assuming equal densities Third, producing many spatially separated flowers with for individuals of different sexual systems, in plants with fewer ovules may facilitate occupation and sampling of separate sexes the average distance between putative an increased volume of air by a plant and thus may mates is greater than in homoecious species and there- increase the probability of capturing pollen grains fore more pollen needs to be produced to outweigh the (Friedman and Barrett 2008). Also, relative to animal- greater transport loss. pollinated species, higher pollen production of wind-pol- In general, studies targeting specific groups have been linated species has been attributed to inefficient pollen stated as essential for understanding of the evolution and transfer (e.g., Whitehead 1969; Faegri and Van Der Pijl maintenance of wind pollination (Friedman and Barrett 1979; Proctor et al. 1996). However, this argument has 2008). Herein we report pollen and ovule production per been challenged by the frequent evolution of wind polli- flower for several species of the hermaphroditic, wind- nation from animal-pollinated ancestors and by empirical pollinated Juncaceae, with special reference to the genus studies (Honig et al. 1992; Harder 2000). Nevertheless, Juncus. Despite its widespread occurrence in many wetland various reasons may account for increased pollen pro- habitats, Juncus is a so far very little studied group. Since duction in wind-pollinated species. First, although wind- the studies of Buchenau (1890, 1892), its reproductive dispersed pollen is not smaller in average diameter than biology has been investigated in detail only rarely (e.g., animal-dispersed pollen (Wodehouse 1935; see data in Michalski and Durka 2007a; Michalski and Durka 2007b). Andrew 1984), it is possibly cheaper to produce because Juncus species are known to produce numerous seeds per it contains less protein (Roulston et al. 2000). Second, at capsule (Kirschner et al. 2002) and, at the same time, least for self-incompatible wind-pollinated species, the pollen production seems quite low. For example, when increase in male fitness gain with increased pollen pro- pollen concentrations in the air were recorded for several duction is not expected to be limited by the transfer sites in Great Britain or southwest Spain, pollen of Junc- capacity of the pollen vector. In contrast, in animal- aceae was found far less frequently than any other ane- pollinated species, the transfer capacity of pollinators is mophilous pollen type (Proctor et al. 1996; Rodriguez likely to limit male fitness gain from increased pollen et al. 2007). More directly, for Juncus pusillus a conspic- production (Charnov 1979; Lloyd 1984; Harder and uous low pollen production has been reported (cited in Pohl Thomson 1989). 1937). In conclusion, Juncus species appear to exhibit low Low ovule and high pollen production should result in P/O ratios in comparison with other wind-pollinated higher pollen–ovule (P/O) ratios in wind-pollinated spe- species. cies compared with animal-pollinated species. Although We relate ovule and pollen production of Juncus species Pohl (1937) concluded that P/O ratios were of similar to wind-pollinated angiosperm species in general and, magnitude, Cruden (2000) and Michalski and Durka using this comprehensive data set, test the following (2009) found P/O ratios on average higher in wind- hypotheses on pollen and ovule production in wind-polli- pollinated species. Nevertheless, relative to animal- nated species: pollinated species, information regarding the reproductive 1. Woody perennials exhibit, on average, higher P/O and floral biology in anemophilous species is scarce ratios than herbaceous species; (Ackerman 2000), and the number of studies concerning 2. Dicliny affects variation in P/O ratios resulting in, on ovule and pollen production in wind-pollinated species is average, lower P/O ratios in homoecious than in quite low (Cruden 2000). Thus, based on more com- monoecious or dioecious species. prehensive data, hypotheses concerning wind-pollinated 123 Pollen and ovule production in wind-pollinatedspecies Author's personal copy 193 Materials and methods monoecious Carex species, all male and female flowers in an inflorescence were counted and the male/female ratio Pollen and ovule