Do soil microbes and abrasion by soil particles influence persistence and loss of physical dormancy in seeds of tropical pioneers?

Abstract

Germination from the soil seed bank (SSB) is an important determinant of species composition in tropical forest gaps, with seed persistence in the SSB allowing trees to recruit even decades after dispersal. The capacity to form a persistent SSB is often associated with physical dormancy, where seed coats are impermeable at the time of dispersal. Germination literature often speculates, without empirical evidence, that dormancy-break in physically dormant seeds is the result of microbial action and/or abrasion by soil particles. We tested the microbial/soil abrasion hypothesis in four widely distributed neotropical pioneer tree species (Apeiba membranacea, Luehea seemannii, Ochroma pyramidale, and Cochlospermum vitifolium). Seeds were buried in five common gardens in a lowland tropical forest in Panama, and recovered at 1, 3, 6, and 12 months after burial. Seed permeability, microbial infection, seed coat thickness, and germination were measured. Parallel experiments compared the germination fraction of fresh and aged seeds without soil contact, and in seeds as a function of seed permeability. Contrary to the microbial/soil abrasion hypothesis the proportion of permeable seeds, and of seeds infected by cultivable microbes, decreased as a function of burial duration. Furthermore, seeds stored in dark and dry conditions for 2 years showed a higher proportion of seed germination than fresh seeds in identical germination conditions. We determined that permeable seeds of A. membranacea and O. pyramidale had cracks in the chalazal area or lacked the chalazal plug, whereas all surfaces of impermeable seeds were intact. Our results are inconsistent with the microbial/soil abrasion hypothesis of dormancy loss and instead suggest the existence of multiple dormancy phenotypes, where a fraction of each seed cohort is dispersed in a permeable state and germinates immediately, while the impermeable seed fraction accounts for the persistent SSB. Thus, we conclude that fluctuations in the soil temperature in the absence of soil abrasion and microbial infection are sufficient to break physical dormancy on seeds of tropical pioneer trees.

Keywords: Barro Colorado Island; germination cue; physical dormancy; pioneer plants; seed dormancy loss; seed persistence; soil seed bank.

FIGURE 1

Scanning electron microscopy images of the surfaces of fresh seeds (A, Apeiba; C, Luehea; E, Ochroma; G, Cochlospermum) and longitudinal sections of seeds (B, Apeiba; D, Luehea; F, Ochroma; H, Cochlospermum). Scale bar = 1 mm. An asterisk highlights the chalazal area when visible.

FIGURE 2

Percentage of seeds retrieved at different time intervals. Seed decay is equivalent to the total number of seeds buried (i.e., 100%), minus the number of seeds recovered successfully at each time. Error bars correspond to SD.

FIGURE 3

Percentage of dormant seeds (black) and germinable seeds (gray) for fresh seeds; 2 years old, laboratory-stored seeds; and seeds successfully recovered at different time intervals after burial. Numbers at the top of each bar represent the number of seeds examined for fresh (never buried), laboratory-stored (never buried), and buried seeds (i.e., the number of seeds retrieved from the common garden experiment and used for the germination experiment).

FIGURE 4

Percentage of seeds infected by cultivable fungi (gray) and seeds without detectable infection (black) for fresh (unburied) seeds, and seeds successfully recovered at different time intervals following burial. Numbers at the top of each bar represent the number of seeds examined for fresh seeds (never buried), and buried seeds (i.e., the number of seeds retrieved from the common garden experiment and used for assessing microbial growth).

FIGURE 5

Percentage of seeds infected by cultivable bacteria (gray) and seeds without detectable infection (black) for fresh (unburied) seeds, and seeds successfully recovered at different time intervals following burial. Numbers at the top of each bar represent the number of seeds examined for fresh seeds (never buried), and buried seeds (i.e., the number of seeds retrieved from the common garden experiment and used for assessing microbial growth).

FIGURE 6

Percentage of permeable seeds (gray) and impermeable seeds (black) for fresh (unburied) seeds, and seeds successfully recovered at different time intervals after burial. Numbers at the top of each bar represent the number of seeds examined for fresh seeds (never buried), and buried seeds (i.e., the number of seeds retrieved from the common garden experiment and used to measure permeability).

FIGURE 7

Scanning electron microscopy images revealing the time course of chalazal plug breakage over 5 days for Apeiba seeds (A–D) and Ochroma seeds (E–H). At the onset of the experiment, seeds of Apeiba (A) and Ochroma (E) previously determined as impermeable had no evidence of cracks on the chalazal area, and the chalazal plug was attached to the seed surface. When seeds were exposed to full sun over 5 days, a gradual release of dormancy was observed as a progressive lifting of the chalazal plug in seeds of Apeiba (B–D) and Ochroma (F–H). Scale bar = 1 mm.

FIGURE 8

Conceptual model summarizing seed persistence and germination in tropical forest species with physically dormant seeds dispersed to (A) the understory or (B) gaps.