A major trade-off between structural and photosynthetic investments operative across plant and needle ages in three Mediterranean pines

Abstract

Pine (Pinus) species exhibit extensive variation in needle shape and size between juvenile (primary) and adult (secondary) needles (heteroblasty), but few studies have quantified the changes in needle morphological, anatomical and chemical traits upon juvenile-to-adult transition. Mediterranean pines keep juvenile needles longer than most other pines, implying that juvenile needles play a particularly significant role in seedling and sapling establishment in this environment. We studied needle anatomical, morphological and chemical characteristics in juvenile and different-aged adult needles in Mediterranean pines Pinus halepensis Mill., Pinus pinea L. and Pinus nigra J. F. Arnold subsp. salzmannii (Dunal) Franco hypothesizing that needle anatomical modifications upon juvenile-to-adult transition lead to a trade-off between investments in support and photosynthetic tissues, and that analogous changes occur with needle aging albeit to a lower degree. Compared with adult needles, juvenile needles of all species were narrower with 1.6- to 2.4-fold lower leaf dry mass per unit area, and had ~1.4-fold thinner cell walls, but needle nitrogen content per dry mass was similar among plant ages. Juvenile needles also had ~1.5-fold greater mesophyll volume fraction, ~3-fold greater chloroplast volume fraction and ~1.7-fold greater chloroplast exposed to mesophyll exposed surface area ratio, suggesting overall greater photosynthetic activity. Changes in needle traits were similar in aging adult needles, but the magnitude was generally less than the changes upon juvenile to adult transition. In adult needles, the fraction in support tissues scaled positively with known ranking of species tolerance of drought (P. halepensis > P. pinea > P. nigra). Across all species, and needle and plant ages, a negative correlation between volume fractions of mesophyll and structural tissues was observed, manifesting a trade-off between biomass investments in different needle functions. These results demonstrate that within the broad trade-off, juvenile and adult needle morphophysiotypes are separated by varying investments in support and photosynthetic functions. We suggest that the ecological advantage of the juvenile morphophysiotype is maximization of carbon gain of establishing saplings, while adult needle physiognomy enhances environmental stress tolerance of established plants.

Structural controls on photosynthetic capacity through juvenile‐to‐adult transition and needle ageing in Mediterranean pines

“…In each species, five mature plants at full sunlight were randomly selected for sampling. The trees were 90–100 years old and 15–21 m tall (Kuusk et al., for species averages). Terminal branchlets without cones (one branch from each individual tree) were taken from the southern part of the upper canopy (average seasonal integrated quantum flux density of ca.…”

“…Here, we hypothesized that these trait differences result in concomitant variations in needle photosynthetic capacity and that the alteration in needle photosynthetic potentials is driven by the trade‐off between support and photosynthetic investments demonstrated in Kuusk et al. (), and furthermore, that the greater structural robustness in adult needles is associated with a stronger limitation of photosynthesis by mesophyll diffusion conductance.…”

“…Particularly large trait alterations occur upon juvenile‐to‐adult transition, a change called heteroblasty (Zotz, Wilhelm, & Becker, ). Heteroblastic modifications in foliage morphology are especially large in pine species (Boddi, Bonzi, & Calamassi, ; Climent, San‐Martín, Chambel, & Mutke, ; Kuusk, Niinemets, & Valladares, ; Mediavilla et al., ; Pardos, Calama, & Climent, ). Juvenile (primary) pine needles are solitary and have different cross‐sectional shape, ellipsoidal or rhomboidal, compared to adult (secondary) needles that have semi‐elliptical (two‐needled species) or sectorial (species with three or more needles in fascicles) shape (Climent, Aranda, Alonso, Pardos, & Gil, ; Kuusk et al., ).…”

“…Heteroblastic modifications in foliage morphology are especially large in pine species (Boddi, Bonzi, & Calamassi, ; Climent, San‐Martín, Chambel, & Mutke, ; Kuusk, Niinemets, & Valladares, ; Mediavilla et al., ; Pardos, Calama, & Climent, ). Juvenile (primary) pine needles are solitary and have different cross‐sectional shape, ellipsoidal or rhomboidal, compared to adult (secondary) needles that have semi‐elliptical (two‐needled species) or sectorial (species with three or more needles in fascicles) shape (Climent, Aranda, Alonso, Pardos, & Gil, ; Kuusk et al., ). In addition, needle linear dimensions, thickness and width, and needle dry mass per unit area are typically lower in juvenile needles (Boddi et al., ; Kuusk et al., ; Mediavilla et al., ; Pardos et al., ).…”

“…Differently from European pines in wetter climates where juvenile needles are present in up to 1‐year‐old seedlings, young Mediterranean pines typically carry juvenile needles longer, for 2–3 years (Climent, San‐Martín, et al., ), suggesting that heteroblastic differences constitute an important seedling adaptation in Mediterranean highly stressful environments. We have previously reported that juvenile needles have lower needle density, greater fraction of mesophyll tissue in needles, thinner mesophyll cell walls and greater chloroplast to exposed mesophyll cell wall surface area, while secondary needles in adult trees are characterized by the opposite suite of these traits (Kuusk et al., ). Here, we hypothesized that these trait differences result in concomitant variations in needle photosynthetic capacity and that the alteration in needle photosynthetic potentials is driven by the trade‐off between support and photosynthetic investments demonstrated in Kuusk et al.…”