Impacts of spring temperature on the duration of high light prior to canopy closure for three forest herbs

Resource Division in an Understory Herb Community: Responses to Temporal and Microtopographic Gradients

In temperate deciduous forests, the short period of high light in spring, prior to canopy closure, is crucial for annual carbon gain of spring understorey plants. However, if the vegetative phenology of deciduous trees and spring herbs respond differently to climate warming, the duration of this high light period might be altered. Here, we present the first field‐based study of the impact of spatial and inter‐annual climate variation on the duration of the high light period for herbaceous spring understorey plants based on direct measurements of leaf phenology. For the tree canopy and two understorey species, Trillium erectum and Erythronium americanum, we estimated phenology using automated cameras from 2017 to 2023 along an elevational gradient in Québec, Canada. Direct observations of leaf phenology allowed us to avoid an unlikely assumption in some previous studies (which were based on flowering time): temperature independence of the delay between leaf‐out and flowering. For both understorey species and the tree canopy, leaf phenology was sensitive to spatial and temporal variation in spring temperature; earlier leaf expansion occurred at warmer sites and in warmer years. Temporal variation in spring temperature had a stronger effect on understorey than canopy phenology, such that warmer temperatures were associated with an increase in the duration of high spring light, especially at high elevation. Across the spatial (elevational) temperature gradient, temperature sensitivity of one understorey species (T. erectum) was weaker than that for the canopy. Thus, the combination of warmer conditions and different canopy tree species at low elevation was associated with a shorter duration of high spring light. Synthesis. Effects of climate warming on phenological escape of spring understorey plants are likely to be small or positive. Results for temporal temperature suggest that over years or decades (while tree canopy composition remains constant), understorey plants should benefit from a warming‐induced prolongation of the high light period. In contrast, results for spatial temperature suggest that, at high elevation, long‐term warming and associated shifts in canopy composition might shrink the time window of high light, although an increase in deciduous tree cover would increase the magnitude of light availability.

Spring ephemerals in the Central Appalachians are a key component of deciduous forest communities and can be indicators of shifting phenology due to climate changes in this ecosystem. The objectives of this study were to (1) determine if there have been any changes in date of flowering for the Cutleaf Toothwort (Cardamine concatenata) and Yellow Trout Lily (Erythronium americanum) in West Virginia over the last 111 years; (2) determine which climatic factors affect the blooming date of these perennial, spring ephemeral wildflowers; and (3) evaluate the effect of elevation on changing blooming dates using herbarium specimens and photographs from 1904 to 2015. Both species are widespread throughout the woodlands of eastern North America. Both species have significantly advanced their spring flowering over the last century (overline{x} = 0.91 days/decade). Spring temperature was the strongest predictor of blooming date (2.91 and 3.44 days earlier/1 °C increase in spring temperature, respectively). Flowers at < 500 m elevation bloomed earlier and demonstrated a stronger shift in flowering date over time than flowers at > 1000 m elevations. Lower elevations, higher spring and winter temperatures, and low amounts of precipitation were associated with earlier spring flowering. This research demonstrates the plasticity of phenological response to a variety of climatic variables, the usefulness of using herbarium specimens to reconstruct flowering dates over a topographically variable area, and the contrasting effects of climate change on high elevation regions of West Virginia.

We investigated the impact of overstory tree leaf phenology on growth rates, carbon allocation pattern, and fruit characteristics in the spring flowering species, Trillium erectum (Liliaceae). Air temperature, overstory canopy closure, and T. erectum phenology were monitored at three locations following a latitudinal gradient in Québec, Canada. Northern sugar maple trees leaf out at cooler temperatures than more southern populations, while Trillium development was initiated at the same soil temperature irrespective of the latitude. Therefore, in northern areas, the time between initiation of T. erectum leaf expansion and canopy closure was shorter than in southern areas, which left less time for northern plants to accumulate reserves before canopy closure. Differences in growth patterns were noted between T. erectum populations. From a south-north gradient, investment to reproduction, total plant biomass, and annual growth rate decreased, while specific leaf area and stem height increased, indicating shade acclimation. The length of the high light period in early spring seems to be a determinant for spring flowering plants' growth and reproduction and may explain the northern distribution limit of some of these species.

Observations were made in a sugar maple (Acer saccharum Marsh.) stand on the phenological response of three geophytes, Claytonia caroliniana, Erythronium americanum, and Trillium erectum, to solar radiation and temperature. The three species started development when the ground was partly covered with snow. The peak of the leafing and flowering stages occurred prior to the lead development of the maple canopy. Two of the geophytes, Claytonia and Erythronium, completed their life cycle prior to leaf development in the canopy. The life cycles appear to be strongly influenced by temperature and solar radiation.

Plantation under the forest is a good way of agroforestry, but the canopy closure has a great influence on understory herbs’ growth. In the study, different canopy closures of Phyllostachys pubescens forests were set up to explore its influence on the growth of Ilex latifolia Thunb. The photosynthetic characteristics of Ilex latifolia leaves under different canopy closures were determined by Li-6400 portable photosynthetic system. The results showed that the net photosynthetic rate curve of Ilex latifolia leaves of T1 (canopy closure of 0.56) was bimodal with an obvious "midday depression" phenomenon, while the net photosynthetic rate curves of T2 (canopy closure of 0.72) and T3 (canopy closure of 0.86) were unimodal. The results of light response curve showed that the photosynthetically active radiation and transpiration rate reduced with the increasing of canopy closures. The photosynthetically active radiation, transpiration rate, stomatal conductance, and net photosynthetic rate of Ilex latifolia leaves of T2 were higher than those of T3. Although the net photosynthetic rate of T2 was lower than that of T1, it had no obvious photo-inhibition which affected plant growth. Overall, the canopy closure of 0.72 was more suitable for the growth of Ilex latifolia. The herb plantation in the bamboo forest should be considered with the canopy closure for a better growth.

Life-history traits explain rapid colonization of young post-agricultural forests by understory herbs

Seasonal patterns of photosynthesis and respiration of single leaves of four understory perennial herbs in deciduous forests were investigated in relation to their leaf growth and light conditions on the forest floor.Anemone flaccida shows rapid growth of leaf area and high rates of gross photosynthesis at light saturation (Psat) in its early stage of development. Its photosynthetic activity is restricted to a brief period of high light intensity before the closure of overstory canopies.Disporum smilacinum possesses light-photosynthesis curves of the shade-leaf type throughout its whole growing period. A shading experiment has shown that this plant is low-light adapted and can utilize weak light efficiently. The light-photosynthesis curve ofSyneilesis palmata shifts from the sun-leaf type to the shade-leaf type in response to the seasonal change of light regime on the forest floor. Evergreen leaves ofPyrola japonica have three year longevity, and light-photosynthesis curves of the shade-leaf type. They maintain some photosynthetic activity even in late autumn and winter.

Windthrow and salvage logging in an old-growth hemlock-northern hardwoods forest

The phenologies of co‐occurring trees and spring‐blooming understory herbs in northeastern North American hardwood forests appear to be regulated by different environmental drivers – air temperature and soil temperature/snowpack, respectively. Accordingly, it has been hypothesized that climate change–driven asymmetry in the advancement of canopy leaf‐out relative to the timing of understory growth could reduce photosynthetic rates and reproductive success of understory herbs through greater early‐season shading. To determine whether trees and spring‐flowering forest herbs are advancing their phenologies at different rates with respect to increasing global temperatures, we examined the phenological responses to warming of 10 species of trees and 11 species of spring‐flowering forest herbs (8045 observations from 965 sites) in northeastern North America using 13 years of data collected by citizen scientists under the auspices of the USA‐National Phenology Network. Contrary to expectation, the degree of advancement of leaf‐out as a function of temperature was greater in spring‐flowering forest herbs than in trees, with a mean response rate of −4.9 days/°C (95% BCI [−5.2, −4.6]) for spring‐flowering forest herbs vs. −3.3 days/°C (95% BCI [−3.5, −3.1]) for trees. However, the response to temperature was not consistent across the latitudinal range, with spring‐flowering forest herbs responding more strongly to warming than trees at middle (40–44°N) and higher (45–48°N) latitudes but not at lower latitudes (35–39°N). Synthesis . In contrast to previous suggestions, our study shows spring‐flowering forest herbs advancing their phenology at a higher rate than trees with respect to warming through most of the latitudinal range investigated, which could translate into a longer growing season and increased carbon uptake for spring‐flowering forest herbs as spring temperatures rise.

One of the best-documented ecological responses to climate warming involves temporal shifts of phenological events. However, we lack an understanding of how phenological responses to climate change vary among populations of the same species. Such variability has the potential to affect flowering synchrony among populations and hence the potential for gene flow. To test whether an earlier start of the growing season affects the potential for gene flow among populations, we quantified the distributions of flowering times of two spring-flowering plants (Trillium erectum and Erythronium americanum) over 6 years along an elevational gradient. We developed a novel model-based metric of potential gene flow between pairs of populations to quantify the potential for pollen-mediated gene flow based on flowering phenology. Earlier onset of spring led to greater separation of peak flowering dates across the elevational gradient for both species investigated, but was only associated with a reduction in potential gene flow in T. erectum, not E. americanum. Our study suggests that climate change could decrease gene flow via phenological separation among populations along climatic gradients. We also provide a novel method for quantifying potential pollen-mediated gene flow using data on flowering phenology, based on a quantitative, more biologically interpretable model than other available metrics.

Soil and sugar maple response 15 years after dolomitic lime application

Main conclusionEffects of a low aluminum (Al) dose were characterized. The Al supplement inhibited root growth but enhanced leaf growth in maize lines with different Al sensitivities.High levels of Al are phytotoxic especially in acidic soils. The beneficial effects of low Al levels have been reported in some plant species, but not in maize. Maize is relatively more sensitive to Al toxicity than other cereals. Seedlings, at the three leaf stage, of four Chinese maize foundation parent inbred lines with different Al tolerances, were exposed to complete Hoagland’s nutrient solution at pH 4.5 supplemented with 48 μM Al3+ under controlled growth conditions, and then the Al stress (AS) was removed. The leaf and root growth, root cell viability, superoxide dismutase (SOD), peroxidase (POD), catalase (CAT), ions (K+, Ca++ and Mg++), photosynthetic rate and chlorophyll, protein and malondialdehyde contents in tissues were assayed. In conclusion, a low Al dose inhibits root growth but enhances leaf growth in maize. The Al-promoted leaf growth is likely a result of increased protein synthesis, a lowered Ca++ level, and the discharge of the growth-inhibitory factors. The Al-promoted leaf growth may be a ‘memory’ effect caused by the earlier AS in maize. Al causes cell wall rupture, and a loss of K+, Ca++ and Mg++ from root cells. CAT is an auxiliary antioxidant enzyme that works selectively with either SOD or POD against AS-related peroxidation, depending on the maize tissue. CAT is a major antioxidant enzyme responsible for root growth, but SOD is important for leaf growth during AS and after its removal. Our results contribute to understanding how low levels of Al affect maize and Al-resistant mechanisms in maize.

Photosynthetic responses to simulated sunflecks (lightflecks) were measured in four understory herbs with a continuum of phenologies (spring green: Erythronium americanum and Podophyllum peltatum; summer green: Arisaema triphyllum and Smilacina racemosa). A light response curve was measured under natural light for each species to quantify the PPFD at light saturation, light‐saturated photosynthetic rate, light compensation point, and dark respiration. Species were compared for the PPFD required to maintain photosynthetic induction. The loss of photosynthetic induction for the three most shade‐tolerant species was determined by measuring their photosynthetic response to lightflecks following different periods in noninducing conditions. Early spring herbs, e.g., E. americanum, responded as full‐sun plants with a higher light compensation point and greater net photosynthesis at light saturation. The PPFD required to maintain an induced photosynthetic state was significantly greater in spring‐green herbs than in summer‐green herbs. Smilacina racemosa and A. triphyllum maintained a high state of induction when exposed to PPFD characteristic of an eastern North American deciduous forest understory. The loss of photosynthetic induction differed among the species. Podophyllum peltatum and S. racemosa exhibited greater inductive loss corresponding to RuBP regeneration, while A. triphyllum exhibited greater inductive loss corresponding to Rubisco inhibition and to stomatal limitations. Therefore, understory herbs of different phenologies display different photosynthetic responses to sunfleck events.

To date, most herbarium-based studies of phenological sensitivity to climate and of climate-driven phenological shifts fall into two categories: detailed species-specific studies vs. multi-species investigations designed to explain inter-specific variation in sensitivity to climate and/or the magnitude and direction of their long-term phenological shifts. Few herbarium-based studies, however, have compared the phenological responses of closely related taxa to detect: (1) phenological divergence, which may result from selection for the avoidance of heterospecific pollen transfer or competition for pollinators, or (2) phenological similarity, which may result from phylogenetic niche conservatism, parallel or convergent adaptive evolution, or genetic constraints that prevent divergence. Here, we compare two widespread Clarkia species in California with respect to: the climates that they occupy; mean flowering date, controlling for local climate; the degree and direction of climate change to which they have been exposed over the last ∼115 yr; the sensitivity of flowering date to inter-annual and to long-term mean maximum spring temperature and annual precipitation across their ranges; and their phenological change over time. Specimens of C. cylindrica were sampled from sites that were chronically cooler and drier than those of C. unguiculata, although their climate envelopes broadly overlapped. Clarkia cylindrica flowers ∼ 3.5 d earlier than C. unguiculata when controlling for the effects of local climatic conditions and for quantitative variation in the phenological status of specimens. However, the congeners did not differ in their sensitivities to the climatic variables examined here; cumulative annual precipitation delayed flowering and higher spring temperatures advanced flowering. In spite of significant spring warming over the sampling period, neither species exhibited a long-term phenological shift. Precipitation and spring temperature interacted to influence flowering date: the advancing effect on flowering date of high spring temperatures was greater in dry than in mesic regions, and the delaying effect of high precipitation was greater in warm than in cool regions. The similarities between these species in their phenological sensitivity and behavior are consistent with the interpretation that facilitation by pollinators and/or shared environmental conditions generate similar patterns of selection, or that limited genetic variation in flowering time prevents evolutionary divergence between these species.