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.
Summery The water-impermeable seed coat of ‘hard’ seeds is commonly considered a dormancy trait. Seed smell is, however, strongly correlated with seed water content, and hard seeds are therefore olfactionally cryptic to foraging rodents. This is the rationale for the crypsis hypothesis, which proposes that the primary functions of hard seeds are to reduce seed predation and promote rodent seed dispersal. We use a mechanistic model to describe seed survival success of plants with different dimorphic soft and hard seed strategies. The model is based on established empirical–ecological relationships of moisture requirements for germination and benefits of seed dispersal, and on experimentally demonstrated relationships between seed volatile emission, predation and predator escape. We find that water-impermeable seed coats can reduce seed predation under a wide range of natural humidity conditions. Plants with rodent dispersed seeds benefit from producing dimorphic soft and hard seeds at ratios where the anti-predator advantages of hard seeds are balanced by the dispersal benefits gained by producing some soft seeds. The seed pathway predicted from the model is similar to those of experimental seed-tracking studies. This validates the relevance and realism of the ecological mechanisms and relationships incorporated in the model. Synthesis. Rodent seed predators are often also important seed dispersers and have the potential to exert strong selective pressures on seeds to evolve methods of avoiding detection, and hard seeds seem to do just that. This work suggests that water-impermeable hard seeds may evolve in the absence of a dormancy function and that optimal seed survival in many environments with rodent seed predators is obtained by plants having a dimorphic soft and hard seed strategy.
Summary 1.On the west coast of Norway, Turdus spp. (Thrushes) are important dispersal agents of Sorbus aucuparia L. (Rowan) seeds, and avian and mammalian gut treatment often alters seed germination characteristics. In the present study the effects of avian gut treatment on S. aucuparia seeds are described, with emphasis on subsequent seedling growth. 2. Seeds ingested by Turdus spp. and non-ingested control seeds were sown singly or multiply in soil, in pomes, or in bird droppings. 3. Defecated seeds were ≈ 9% heavier than control seeds, and seedling growth was faster from defecated seeds than controls. In addition, differences in the rate of seedling emergence were found, with seedlings from ingested seeds appearing first. 4. The increased growth may be due to seedlings emerging earlier from defecated seeds, giving them an extended growth period at a time of increasing day length. 5. We argue that factors such as seedling growth, rate of seedling emergence and seed mass, in addition to percentage seed germination, are important in determining seedling survival.
In imbibing seeds, resumption of metabolism leads to the unavoidable release of volatile by-products that are perceived as cues by rodent seed predators. The crypsis hypothesis proposes that the primary function of a water-impermeable, hard seed coat is to reduce rodent seed predation by rendering seeds olfactorily cryptic. In an opinion paper, Jayasuriya et al. (2015) find the crypsis hypothesis unscientific and 'not consistent with Darwin's theory of evolution by natural selection'. It is unfortunate that Jayasuriya et al. (2015) did not appreciate that the crypsis hypothesis offers an alternative explanation for the evolution of waterimpermeable seeds: released seed volatiles are cues used by rodents to locate seeds, and variation in seedcoat permeability leading to differences in seed volatile release represents the variable under selection. Furthermore, the sealing of water-impermeable seed coats imposes a cost of increased generation time and, therefore, dormancy-release mechanisms are expected to subsequently evolve in response to local environmental conditions. We also disagree with most other claims by Jayasuriya et al. (2015), who failed to appreciate how species with dimorphic seeds -one morph with permeable and the other with impermeable seed coats -benefit from rodent caching behaviour and population dynamics. We welcome this opportunity to clarify and elaborate on key features and the evolution of water-impermeable seed coats according to the crypsis hypothesis.
Reduced seed exit costs have been suggested to explain advanced seedling emergence and increased seedling growth in Sorbus aucuparia L. (Rosaceae; rowan) following Turdus spp. (Turdidae; thrush) gut passage. In the present study, seed coat tension strength of Turdus merula L. (Turdidae; blackbird) gut-passed and non-ingested control seeds were tested with a diametral compression test. Both maximum load (N) and work (mJ) required for opening the seeds were reduced in gut-passed seeds, although scanning electron microscopy showed no visible differences in seed coat surface structure between treatments. In addition, gut passage increased dry seed weight by 0.64�mg (22%), weight of hydrated seeds by 0.62�mg (16%) and width of hydrated seeds by 0.1�mm (9%). Absorption causing the seed coat to yield more easily to the germinating seedling is proposed as an explanation for the reduction in seed exit costs. For the emerging seedling, the time and force needed to open the seed coat was reduced, thus lowering dispersal and germination costs of S. aucuparia.
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