Climate change spells peril for dioecious plants

Will climate change – and particularly increased aridity – alter the sex ratios of dioecious plants? That’s the question which researchers including those involved with SEGA ask in a paper just published in Nature Plants.

A team led by Kevin Hultine examine existing published literature and data sets to see if forecasted increases in variables such as vapor pressure deficit and reduced water availability will differentially impact male and female demography in dioecious plants (species with separate male and female individuals, along with bi-parental reproduction). They focus on how measures of plant ecophysiology and productivity that depending on gender, respond differently to predicted climate change depending on whether plants are male or female.

What made the researchers ask this question? And why is it important? Because dioecious plant sexes are often spatially separated they may be especially vulnerable to climate change. And with dioecy occurring in 157 flowering plant families worldwide - about one-half of all angiosperm families (flowering plants including shrubs, grasses, herbaceous plants and most trees), significant changes in the sex ratios of this plants species could have wide ranging and profound consequences. Not just for plant communities themselves – but for the many biotic communities that live and depend on them.

The team looked at approximately 200 published studies containing sex ratio estimates for about 250 dioecious species. While this constitutes just over 1% of the approximately 21,000 dioecious species worldwide – it establishes an important baseline for predicting the effects of climate change. Sex ratio bias is present in about half of all species studied. Patterns of sex ratio bias depend on a host of factors (e.g. growth form, clonal habit, pollen and seed dispersal mechanisms) with male-biased sex ratios prevalent in trees  and vines (and associated with biotic pollen dispersal and fleshy fruit development), but generally absent in most annuals, herbs and shrubs. Male-biased sex ratios are nearly twice as frequent as female-biased sex ratios. Long-lived trees that depend on seed dispersal by animals, are far more likely to display male-biased sex ratios whereas plants that rely on abiotic seed dispersal have fairly equal sex ratios.

The impact of climate change on future sex ratios may depend largely on how the sex ratio bias is expressed. For example, sex ratios mainly determined by differential mortality may be much more influenced by climate changes versus those determined by seed and pollen dispersal distances - mortality related to sex differences in plant water relations will likely mean one sex is better equipped to cope with aridity than the other. Climate-related patterns of continental-scale die-offs of woody plants have occurred throughout the globe, largely as a consequence of increased temperature and aridity. The mortality is often mainly due to plant hydraulic failure and – or, carbon starvation.

What emerged from this study is that female dioecious plants are more vulnerable to water stress than males, although the exact relationship depends on a combination of factors including the size and speed of climate change, life history strategies, local adaptation and generation turnover times. So the researchers hypothesize that higher mortality of female individuals is more likely in less favorable habitats or those subjected to episodic disturbance. And since the vast majority of plants will be exposed to greater drought intensity and deleterious increases in temperature with climate change – the conclusion is that males might often be more resilient. With the possibility that extreme male-biased sex ratios are possible in a significant number of populations, the effect that is likely to cascade to dependent community members, especially those specialized on one sex. For example, with Valeriana edulis, female plants supported much higher densities of aphids, aphid predators and aphid-tending ants relative to male plants – and they in turn structure much larger communities of organisms (in this case 90 species of arthropods). So cascading trophic interactions may be a significant consequence of changing climate affecting plant sex ratios.

Long-lived dioecious species such as trees and woody shrubs are likely to be more susceptible to the effects of rapid shifts in climate on their sex ratios because of their long generation turnover times, which restricts the rate at which they can adapt. Higher CO2 concentrations predicted during the next century may lessen the sensitivity of female plants to stress but much research is needed to tease apart the complex interactions.

In summary, researchers anticipate that:
1.    Male dioecious plants will generally be less sensitive to the effects of increased aridity in terms of gas exchange and growth than co-occurring females.
2.    The rate of mortality in female plants will outpace the rate of mortality in co-occurring males, particularly in species where females display a greater physiological sensitivity than males and are burdened with the high cost of fleshy fruit construction to support seed dispersal.
3.    Extreme male-biased sex ratios are most likely to emerge in species that occur in locations where rates of climate change are highest and in long-lived species (trees and woody shrubs).
4.    Cascading effects of the above three factors will affect ecosystem processes and the structure of dependent communities that favor one plant sex over the other.

Full reference:
Climate change perils for dioecious plant species. (in press). Kevin R. Hultine, Kevin C. Grady, Troy E. Wood, Stephen M. Shuster, John C. Stella5 and Thomas G. Whitham. Nature Plant, 109, to be published on 2nd Aug 2016.