The role of maternal age, growth, and environment in shaping offspring performance in an aerial conifer seed bank

Abstract

Premise: Maternal effects have been demonstrated to affect offspring performance in many organisms, and in plants, seeds are important mediators of these effects. Some woody plant species maintain long-lasting canopy seed banks as an adaptation to wildfires. Importantly, these seeds stored in serotinous cones are produced by the mother plant under varying ontogenetic and physiological conditions.

Methods: We sampled the canopy seed bank of a highly serotinous population of Pinus pinaster to test whether maternal age and growth and the environmental conditions during each crop year affected seed mass and ultimately germination and early survival. After determining retrospectively the year of each seed cohort, we followed germination and early survival in a semi-natural common garden.

Results: Seed mass was related to maternal age and growth at the time of seed production; i.e., slow-growing, older mothers had smaller seeds, and fast-growing, young mothers had larger seeds, which could be interpreted either as a proxy of senescence or as a maternal strategy. Seed mass had a positive effect on germination success, but aside from differences in seed mass, maternal age had a negative effect and diameter had a positive effect on germination timing and subsequent survival.

Conclusions: The results highlight the importance of maternal conditions combined with seed mass in shaping seedling establishment. Our findings open new insights in the offspring performance deriving from long-term canopy seed banks, which may have high relevance for plant adaptation.

Keywords: Pinus pinaster; canopy seed bank; germination; maternal effects; recruitment; seed mass; serotiny; survival; transgenerational plasticity.

Figure 1

Photographs of a natural population of Pinus pinaster in Tabuyo del Monte (northwestern Spain). (A) One of the mother trees sampled. (B) An aerial seed bank with serotinous cones from different cohorts. (C) Branch with serotinous cones (see Appendix 1 to complement Figures 1B and 1C). (D) Serotinous cones

Figure 2

Within‐ and between‐mother trees effects of (A) maternal age, (B) centered ring width, and (C) tree diameter on seed mass for the 16 sampled mother trees. The y‐axis represents residual seed mass after accounting for calendar year effects (cohort). Thin black lines show individual linear regressions for each mother tree. The thick black line in each panel was drawn from the estimated parameters in the mixed model when that predictor was significant (Table 1)

Figure 3

Relationship between age and diameter of mother trees. Large points correspond to the mean age of each mother tree; small points represent values for each cohort within trees. The black line was drawn from the estimated parameters of the mixed model fitted (t _10.02 = 63.90, P < 0.001)

Figure 4

Kaplan–Meier estimates of germination probability curves for all trees, illustrating the differences in the germination time between individuals. The vertical distance between 0 and 1 represents the change in cumulative probability of germination as the curve advances