Predestined to be awake

Being able to lie dormant is a huge advantage for a seed but, in the campo rupestre of Brazil, the seeds are unusually impatient.

by Roberta LC Dayrell & Fernando AO Silveira

Most seeds from all over the world have evolved and maintained a precious ecological strategy: not to germinate when all conditions are perfect to do so. This gift, known as seed dormancy, might seem like a Trojan horse that misleads seeds into wasting a clear germination opportunity. Although seeds are meant to germinate, waiting for optimum conditions is often the best strategy for seeds.

Dormancy allows plants to spread germination across time and lower the risk of losing an entire cohort of seedlings due to unpredictable events, such as persistent droughts. Seed dormancy also avoids the death of juveniles by synchronizing germination with suitable timing for seedling establishment in seasonal environments. These benefits help us understand why dormancy is a remarkably dominant trait across all seasonal environments worldwide.

The campo rupestre grassland in eastern Brazil, a short-term seasonal and long-term stable environment, is the only known exception to this rule. What we have found is that the majority of campo rupestre‘s taxa (62.5 %) had non-dormant seeds, the lowest proportion of dormant seeds for any vegetation type on Earth.

Biome-wide percentage of seed dormancy categories among campo rupestre and tropical evergreen forests, tropical semi-deciduous forests, savannas and tropical deciduous forests
Biome-wide percentage of seed dormancy categories among campo rupestre (this study) and tropical evergreen forests, tropical semi-deciduous forests, savannas and tropical deciduous forests (Baskin and Baskin, 2014). D and ND frequencies were significantly different among all vegetation zones, except for savannas and tropical deciduous forests, according to the χ2 test

Another surprising finding is that seeds of campo rupestre are somehow born with a predestined role, leaving little or no room for the influence of contemporary factors. Seed dormancy and quality were found to be strongly associated with species evolutionary history, indicating that closely related species have a very similar behaviour. Further, species traits that are usually good predictors of dormancy in other environments – e.g. seed dispersal time and microhabitat – could not explain any of the observed patterns, providing additional support that long-term stability may have shaped seed dormancy.

Strikingly, seed quality was far more important than dormancy as a cause for the lack of germination in species from campo rupestre. At least half of the seeds produced by 46% of the surveyed populations were embryoless (empty seeds) and/or otherwise non-viable. We think that these findings are part of many peculiarities that are being found for old, climatically-buffered and infertile landscapes (OCBILs). In this context, they highlight that the remarkable phosphorus limitation in OCBILs is often associated with drastic constraints in plant sexual reproduction and could lead to a very poor seed set. This result is somewhat worrisome, since seed-based restoration strategies developed in other vegetation types, may not be effective for restoration of campo rupestre.

Dormancy is a precious gift, but it may cause seeds to be asleep at the switch and demise before they get a chance to germinate. When nutrients are scarce and seeds become expensive, waiting to germinate might be a luxury difficult to afford.

Endemism Hotspots Cover

This article is part of the AoB Special Issue on Endemism Hotspots as Climate Change Refugia, which is free access for a couple of months, then behind the paywall for a while before being free access after February 2017.

Reference

Baskin, C. C., & Baskin, J. M. (1998). Seeds: ecology, biogeography, and evolution of dormancy and germination, 2nd edn. San Diego: Elsevier/Academic Press. http://dx.doi.org/10.1016/B978-012080260-9/50001-4

Dayrell, R. L. C., Garcia, Q. S., Negreiros, D., Baskin, C. C., Baskin, J. M., & Silveira, F. A. O. (2017). Phylogeny strongly drives seed dormancy and quality in a climatically buffered hotspot for plant endemism. Annals of Botany, 119(2), 267–277. https://doi.org/10.1093/aob/mcw163

Hopper, S. D., Silveira, F. A. O., & Fiedler, P. L. (2015). Biodiversity hotspots and OCBIL theory. Plant and Soil, 403(1-2), 167–216. https://doi.org/10.1007/s11104-015-2764-2

Silveira, F. A. O., Negreiros, D., Barbosa, N. P. U., Buisson, E., Carmo, F. F., Carstensen, D. W., … Lambers, H. (2015). Ecology and evolution of plant diversity in the endangered campo rupestre: a neglected conservation priority. Plant and Soil, 403(1-2), 129–152. https://doi.org/10.1007/s11104-015-2637-8