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11 November 2013 Sex-specific flowering patterns and demography of the understorey rain forest tree Iryanthera hostmannii (Myristicaceae)
Abstract

Sexual dimorphism in dioecious plants is a common phenomenon that has received widespread attention, yet the implications for reproductive function and fitness remain poorly understood. Using data from a long-term study of a population of 839 dioecious Iryanthera hostmannii (Myristicaceae ‘nutmeg’) trees in a large permanent plot in a lowland tropical rain forest, we examined the effects of greater investment in reproduction by females compared to males for various aspects of life history. Although male trees often produced more inflorescences than females, total dry mass of flowers was roughly equal in two out of three years for both sexes, implying that any investment differential lies in fruit production. There was no difference in the 12-year relative growth rate of males and females, suggesting that females can compensate somehow for their greater reproductive investment, although there were weak suggestions that mortality might have been greater in females. Male flowers opened slightly earlier in the day than female flowers and were short-lived, lasting at most two nights compared to up to four nights in females. Understanding the interacting effects of resource availability (studied here) and pollen movement (currently unknown in Iryanthera) on reproduction is essential in terms of life history theory. Knowledge of reproductive biology is key in considering the ecology and conservation of tropical forest communities.

Introduction

In a finite world, organisms must allocate acquired resources in a way that maximizes fitness. Resources allocated to growth, survival or reproduction often cannot be reassigned to another function nor serve a dual function. Thus, in plants, trade-offs often exist, such as between allocating to height growth, permitting increased carbon gain, or to seed production, ensuring that reproductive fitness is not zero. Because reproduction is the ultimate goal of any individual, the ‘cost’ of reproduction, usually expressed as a decrease in future growth or survival, has received particular attention from biologists and is central to life history theory.

Studies of life history are often comparative, for example examining differences in resource allocation between annual and perennial plants. Those studies, however, suffer from the fact that such comparisons are between organisms that differ greatly in life history strategy. To better understand how the cost of reproduction affects life history strategy and in particular how reproduction is influenced by the resources allocated to it, we would ideally compare individuals that allocate much to reproduction with those that allocate little, within a single population of related individuals. Dioecious species, those which separate male and female function between different individuals, offer just such a natural experiment. Species with this breeding system usually exhibit sex-related differences in reproductive investment, with females generally allocating more to any one reproductive event than males [1, 2, 3]. Because sex is separated on different plants, male and female functions are independent of each other, and populations of dioecious plants therefore provide an excellent opportunity to examine the influence of reproductive costs on life history strategy.

Many of the observed differences in life history strategy between males and females are caused by this difference in investment in reproduction and have been known for a long time [1, 2]. For example, males often flower more frequently than females [4, 5], flower earlier (both in terms of phenology and size or age) [6, 7, 8, 9], and have faster growth and lower mortality [7, 10]. These strategies in turn usually give rise to male-biased sex ratios [11]. Further, sexual dimorphism in vegetative organs has been observed [2, 12, 13], and each sex may occupy different ‘sub-niches’ within the same environment, usually with females occurring more frequently in high- resource patches [14, 15]. However, these patterns are not observed consistently among all dioecious species, and results from such studies are often inconclusive regarding the influence of resource allocation on reproduction [16]. This confusion may in part be because the trade-off between reproduction and other resource sinks can vary markedly from year to year because of fluctuating resource availability over time [17, 18, 11, 19], and investment in reproduction may vary across temporal, spatial and morphological scales. Long-term studies are necessary to understand these effects. Furthermore, many studies are on short-lived herbaceous plants, and data are lacking for many tropical tree species, even though dioecy is more common in tropical systems than in temperate ones [20].

Dioecious species not only provide a natural experiment to examine how resource allocation patterns differ between the sexes, but also allow us to examine how selection acts differently on males and females to maximise their reproductive fitness [10, 21]. These selection pressures, in turn, may influence allocation patterns. For example, competition between males will favour males that flower at as small a size as possible, because this will likely increase their number of offspring compared to males that delay flowering. Equally, males that start to open their flowers just before the bulk of female flowers open will be selected for because the pollen from these males would likely reach females before pollen from late-opening males. Most previous work on dimorphism in flowering phenology has focused on differences at the whole population level, i.e. do males flower earlier in the season than females? Little work has been carried out on daily phenological patterns at the individual or flower level [22].

In a long-term study of reproduction, growth and demography of the Myristicaceae, a dioecious tropical tree family, Queenborough et al. (2007) [19] documented a large differential in reproductive investment between the sexes in Iryanthera hostmannii. The dry mass of each female fruit was several orders of magnitude greater than a single male flower (1600mg versus 0.48mg). At the tree level this difference was less, but females still invested an order of magnitude more dry mass in reproduction than males (mean total fruit mass per female tree was 91g, whereas mean total flower mass per male tree was 1.4g). This lower cost of reproduction in males resulted in higher flowering frequency of males leading to male biased flowering sex ratios [19]. However, the growth rate analyses presented were limited to only six years of data, and too few individuals died to attempt any analysis of mortality. Since then [19], six more years of demography data have become available. Re-analysing these expanded data will allow us to better address the question of whether higher allocation to reproduction by females is expressed in the long-term