Physical dormancy in seeds: a game of hide and seek?

Abstract

SummaryHistorically, 'physical dormancy', or 'hard seededness', where seeds are prevented from germinating by a water-impermeable seed coat, is viewed as a dormancy mechanism. However, upon water uptake, resumption of metabolism leads to the unavoidable release of volatile by-products, olfactory cues that are perceived by seed predators. Here, we examine the hypothesis that hard seeds are an anti-predator trait that evolved in response to powerful selection by small mammal seed predators.Seeds of two legume species with dimorphic seeds ('hard' and 'soft'), Robinia pseudoacacia and Vicia sativa, were offered to desert hamsters (Phodopus roborovskii) in a series of seed removal studies examining the differences in seed harvest between hard and soft seeds. Volatile compounds emitted by dry and imbibed soft seeds were identified by headspace gas chromatography-mass spectrometry (GC-MS).Fourteen main volatile compounds were identified, and hamsters readily detected both buried imbibed seeds and an artificial 'volatile cocktail' that mimicked the scent of imbibed seeds, but could not detect buried hard or dry soft seeds.We argue that physical dormancy has evolved to hide seeds from mammalian predators. This hypothesis also helps to explain some otherwise puzzling features of hard seeds and has implications for seed dispersal.

The crypsis hypothesis explained: a reply to Jayasuriya et al. (2015)

“…However, even if we accept the hypothesis suggested by Paulsen et al (2013), both hard seeds and soft seeds should be consumed similarly as soon as they are detected. If soft seeds are detected in higher numbers, then they will be consumed in higher numbers, and thus the selective pressure would have already eliminated the soft seeds.…”

“…The crypsis hypothesis also makes predictions about other seed traits associated with water-impermeable hard seeds, explaining general patterns observed in The crypsis hypothesis explained 403 natural populations that would otherwise need ad hoc explanations (Paulsen et al, 2013(Paulsen et al, , 2014. However, as with all general ecological explanations, exceptions to the rule are not only expected, but welcome, since they provide information on the limits of the general pattern.…”

“…Second, there is seasonality in rodent caching behaviour, with highest caching activity in the autumn and declining cache recovery until late spring, when it seems to come to an end (Thompson and Thompson, 1980;Vander Wall, 1990). Third, the findings from the mixed seed experiments (Paulsen et al, 2013, fig. 2b and e, p. 499 and table S3 in the supporting information) demonstrated that water-impermeable hard seeds were left behind during cache harvest.…”

“…Hollander et al, 2012) giving variation both within and between species. Selection by rodents, assuming that variation in seed-coat permeability is heritable, is expected to result in directional selection towards seeds releasing less volatiles until we end up with water-impermeable olfactionally cryptic seeds (Vander Wall, 2003;Paulsen et al, 2013). Since these seeds are likely to have evolved from an ancestor with PD (Willis et al, 2014), the predator escape benefit of producing waterimpermeable seeds must exceed the cost of increased generation time presumably imposed on this new seed morph.…”

“…Inspired by the work on how rodents use smell to locate imbibed seeds by Vander Wall and others (e.g. Howard and Cole, 1967;Johnson and Jorgensen, 1981;Vander Wall, 1991, 1993a, b, 1995, 2000, 2010Jorgensen, 2001;Vander Wall and Jenkins, 2003;Vander Wall et al, 2005), we revisited the dormancy hypothesis for the evolution of hard seeds, which led us to propose the crypsis hypothesis as an alternative explanation for the evolution of hardseededness, suggesting that the primary function of waterimpermeable hard seeds is their ability to reduce seed predation (Paulsen et al, 2013). We demonstrated that buried water-impermeable hard seeds are difficult to find for rodent seed predators that use volatiles as cues to locate seeds (Paulsen et al, 2013, andsee also Vander Wall, 2003).…”