Understory plants evade shading in a temperate deciduous forest amid climate variability by shifting phenology in synchrony with canopy trees.

Global warming is leading understory and canopy plant communities of temperate deciduous forests to grow leaves earlier in spring and drop them later in autumn. If understory species extend their leafy seasons less than canopy trees, they will intercept less light. We look for mismatched phenological shifts between canopy and understory in 28 years (1995-2022) of weekly data from Trelease Woods, Urbana, IL, USA. The observations cover 31 herb species of contrasting seasonality (for 1995-2017), three sapling species, and the 15 most dominant canopy tree species for all years, combined with solar radiation, temperature and canopy light transmittance data. We estimate how understory phenology, cold temperatures, canopy phenology, and solar radiation have individually limited understory plants' potential light interception over >2 decades. Understory and canopy phenology were the two factors most limiting to understory light availability, but which was more limiting varied greatly among species and among/within seasonality groups; solar radiation ranked third and cold fourth. Understory and canopy phenology shifts usually occurred in the same direction; either both strata were early or both were late, offsetting each other's effects. The four light-limiting factors combined showed significant temporal trends for six understory species, five toward less light interception. Warmer springs were significantly associated with shifts toward more light interception in three sapling species and 19 herb species. Canopy phenology became more limiting in warmer years for all three saplings species and 31 herb species. However, in aggregate, these variables mostly offset one another; only one sapling and seven herb species showed overall significant (and negative) relationships between light interception and spring temperature. The few understory species mismatched with canopy phenology due to changing climate are likely to intercept less light in future warmer years. The few species with data for carbon assimilation show broadly similar patterns to light interception.

Reconstructing patterns of temperature, phenology, and frost damage over 124 years: spring damage risk is increasing.

Climate change, with both warmer spring temperatures and greater temperature fluctuations, has altered phenologies, possibly leading to greater risk of spring frost damage to temperate deciduous woody plants. Phenological observations of 20 woody species from 1993 to 2012 in Trelease Woods, Champaign County, Illinois, USA, were used to identify years with frost damage to vegetative and reproductive phases. Local temperature records were used in combination with the phenological observations to determine what combinations of the two were associated with damage. Finally, a long-term temperature record (1889-1992) was evaluated to determine if the frequency of frost damage has risen in recent decades. Frost < or = -1.7 degrees C occurred after bud-break in 14 of the 20 years of observation. Frost damage occurred in five years in the interior and in three additional years at only the forest edge. The degree of damage varied with species, life stage, tissue (vegetative or reproductive), and phenological phase. Common features associated with the occurrence of damage to interior plants were (1) a period of unusual warm temperatures in March, followed by (2) a frost event in April with a minimum temperature < or = -6.1 degrees C with (3) a period of 16-33 days between the extremes. In the long-term record, 10 of 124 years met these conditions, but the yearly probability of frost damage increased significantly, from 0.03 during 1889-1979 to 0.21 during 1980-2012. When the criteria were "softened" to < or = -1.7 degrees C in April and an interval of 16-37 days, 31 of 124 years met the conditions, and the yearly damage probability increased significantly to 0.19 for 1889-1979 and 0.42 for 1980-2012. In this forest, the combination of warming trends and temperature variability (extremes) associated with climate change is having ecologically important effects, making previously rare frost damage events more common.

Incorporating animal behavior into seed dispersal models: implications for seed shadows.

Seed dispersal fundamentally influences plant population and community dynamics but is difficult to quantify directly. Consequently, models are frequently used to describe the seed shadow (the seed deposition pattern of a plant population). For vertebrate-dispersed plants, animal behavior is known to influence seed shadows but is poorly integrated in seed dispersal models. Here, we illustrate a modeling approach that incorporates animal behavior and develop a stochastic, spatially explicit simulation model that predicts the seed shadow for a primate-dispersed tree species (Virola calophylla, Myristicaceae) at the forest stand scale. The model was parameterized from field-collected data on fruit production and seed dispersal, behaviors and movement patterns of the key disperser, the spider monkey (Ateles paniscus), densities of dispersed and non-dispersed seeds, and direct estimates of seed dispersal distances. Our model demonstrated that the spatial scale of dispersal for this V. calophylla population was large, as spider monkeys routinely dispersed seeds >>100 m, a commonly used threshold for long-distance dispersal. The simulated seed shadow was heterogeneous, with high spatial variance in seed density resulting largely from behaviors and movement patterns of spider monkeys that aggregated seeds (dispersal at their sleeping sites) and that scattered seeds (dispersal during diurnal foraging and resting). The single-distribution dispersal kernels frequently used to model dispersal substantially underestimated this variance and poorly fit the simulated seed-dispersal curve, primarily because of its multimodality, and a mixture distribution always fit the simulated dispersal curve better. Both seed shadow heterogeneity and dispersal curve multimodality arose directly from these different dispersal processes generated by spider monkeys. Compared to models that did not account for disperser behavior, our modeling approach improved prediction of the seed shadow of this V. calophylla population. An important function of seed dispersal models is to use the seed shadows they predict to estimate components of plant demography, particularly seedling population dynamics and distributions. Our model demonstrated that improved seed shadow prediction for animal-dispersed plants can be accomplished by incorporating spatially explicit information on disperser behavior and movements, using scales large enough to capture routine long-distance dispersal, and using dispersal kernels, such as mixture distributions, that account for spatially aggregated dispersal.

Intraspecific variation in seed dispersal of a Neotropical tree and its relationship to fruit and tree traits.

The distribution of wind-dispersed seeds around a parent tree depends on diaspore and tree traits, as well as wind conditions and surrounding vegetation. This study of a neotropical canopy tree, Platypodium elegans, explored the extent to which parental variation in diaspore and tree traits explained (1) rate of diaspore descent in still air, (2) distributions of diaspores dispersed from a 40-m tower in the forest, and (3) natural diaspore distributions around the parent tree. The geometric mean rate of descent in still air among 20 parents was highly correlated with geometric mean wing loading(1/2) (r = 0.84). However, diaspore traits and rate of descent predicted less variation in dispersal distance from the tower, although descent rate(-1) consistently correlated with dispersal distance. Measured seed shadows, particularly their distribution edges, differed significantly among six parents (DBH range 62-181 cm) and were best fit by six separate anisotropic dispersal kernels and surveyed fecundities. Measured rate of descent and tree traits, combined in a mechanistic seed dispersal model, did not significantly explain variation among parents in natural seed dispersal distances, perhaps due to the limited power to detect effects with only six trees. Seedling and sapling distributions were at a greater mean distance from the parents than seed distributions; saplings were heavily concentrated at far distances. Variation among parents in the distribution tails so critical for recruitment could not be explained by measured diaspore or tree traits with this sample size, and may be determined more by wind patterns and the timing of abscission in relation to wind conditions. Studies of wind dispersal need to devote greater field efforts at recording the "rare" dispersal events that contribute to far dispersal distances, following their consequences, and in understanding the mechanisms that generate them.

Irregular rain cues and the germination and seedling survival of a Panamanian shrub (Hybanthus prunifolius).

Seeds of the Panamanian shrub, Hybanthus prunifolius (Schult.) Schulze (Violaceae) are dispersed at different times in different years ((March to June) and are exposed to the irregular rainfall of the dry season in some years. Fluctuations in soil moisture in the dry season represent suboptimal conditions for germination and seedling survival. There are no mechanisms to prevent germination prior to the arrival of consistent rains in the wet season.Among three natural cohorts of seeds followed in two years, the cohort experiencing the longest time from sowing to consistent rains had the highest germination, but it also had the longest time lag from sowing to, beginning of germination, longest germination period, and lowest survival of seedlings 3 months after sowing.Seeds were also induced experimentally to germinate under 14 different moisture patterns. The patterns encompassed 1) varying lengths of moisture before a dry period, 2) inconsistent moisture, and 3) varying lengths of dryness prior to any moisture.Mortality of seeds by fungal infection occurred if the wet period was delayed. But germination was less affected by fluctuations than was seedling survival. Length of the first wet period and frequency of occurrence of the wet period both affected germination levels. Survival and development of seedlings was influenced by the number of days exposed to dry conditions and by the stage of development at the beginning of the dry period. Young seedlings suffered attrition due to drought stress, and older seedlings died from fungal attack.Results from field and experimental sowing of seeds both indicate that this perennial species has minimal defense against germination when conditions are suboptimal for seedling survival. Undoubtedly there is more recruitment in some years than in others.

Pathogen mortality of tropical tree seedlings: experimental studies of the effects of dispersal distance, seedling density, and light conditions.

We present results of two experiments designed to identify the relative importance of dispersal distance, seedling density, and light conditions on pathogen-caused mortality of tropical tree seedlings. The field experiment on Barro Colorado Island, Panama, demonstrated that both an increase in dispersal distance and a decrease in seedling density reduce levels of damping-off disease among seedlings of Platypodium elegans, and that there is an interaction between the two factors. The results indicated significant variation among sites in pathogen activity and suggested that seedlings are more vulnerable to disease when establishing around their parent tree than around other conspecific trees.The second experiment in a screened enclosure used potted seedlings of 18 wind-dispersed tree species exposed to two levels of sunlight and seedling density. The results indicated that environmental conditions similar to those in light-gaps significantly reduce pathogen activity. They also confirmed that high seedling density increases disease levels, especially under shaded conditions.Seedlings of 16 of the 18 species experienced pathogencaused mortality, but in widely varying amounts. Seed weight was not a good predictor of a species' vulnerability to pathogens. Adult wood density, an indicator of growth rate and successional status, was inversely correlated with a species' vulnerability to pathogens. Fast-growing, colonizing species, whose seedlings require light-gaps, lacked strong resistance to seedling pathogens, relative to slow-growing species able to tolerate shade and escape seedling pathogens. We discuss these results in the context of seed dispersal as a means of escaping from seedling pathogens.

Differences in leaf phenology between juvenile and adult trees in a temperate deciduous forest.

In a deciduous forest, differences in leaf phenology between juvenile and adult trees could result in juvenile trees avoiding canopy shade for part of the growing season. By expanding leaves earlier or initiating senescence later than canopy trees, juvenile trees would have some period in high light and therefore greater potential carbon gain. We observed leaf phenology of 376 individuals of 13 canopy tree species weekly over 3 years in a deciduous forest in east central Illinois, USA. Our objectives were: (1) to quantify for each species the extent of differences in leaf phenology between juvenile and conspecific adult trees; and (2) to determine the extent of phenological differences between juvenile Aesculus glabra Willd. and Acer saccharum Marsh. trees in understory and gap microhabitats. All species displayed phenological differences between life stages. For 10 species, bud break was significantly earlier, by an average of 8 days, for subcanopy individuals than for canopy individuals. In 11 species, completion of leaf expansion was earlier, by an average of 6 days, for subcanopy individuals than for canopy individuals. In contrast, there were no significant differences between life stages for start of senescence in 10 species and completion of leaf drop in nine species. For eight species, leaf longevity was significantly greater for subcanopy individuals than for canopy individuals by an average of 7 days (range = 4-10 days). Leaf phenology of subcanopy individuals of both Aesculus glabra and Acer saccharum responded to gap conditions. Leaf longevity was 11 days less in the understory than in gaps for Aesculus glabra, but 14 days more in the understory than in gaps for Acer saccharum. Therefore, leaf phenology differed broadly both between life stages and within the juvenile life stage in this community. A vertical gradient in temperature sums is the proposed mechanism explaining the patterns. Temperature sums accumulated more rapidly in the sheltered understory than in an open elevated area, similar to the canopy. Early leaf expansion by juvenile trees may result in a period of disproportionately higher carbon gain, similar to gains made during summer months from use of sun flecks.

Early spring leaf out enhances growth and survival of saplings in a temperate deciduous forest.

Saplings of many canopy tree species in winter deciduous forests receive the major portion of their light budget for their growing season prior to canopy closure in the spring. This period of high light may be critical for achieving a positive carbon (C) gain, thus contributing strongly to their growth and survival. This study of saplings of Aesculus glabra and Acer saccharum in Trelease Woods, Illinois, USA, tested this hypothesis experimentally by placing tents of shade cloth over saplings during their spring period of high light prior to canopy closure in three consecutive years. Leaf senescence began 16 days (year 0) and 60 days (year 1) earlier for shaded A. glabra saplings than control saplings. No change in senescence occurred for A. saccharum. The annual absolute growth in stem diameter of both species was negligible or negative for shaded saplings, but positive for control saplings. Only 7% of the shaded A. glabra saplings were alive after 2 years, while all control saplings survived for 3 years; only 20% of the shaded A. saccharum saplings survived for 3 years, while 73% of control saplings were alive after the same period. Early spring leaf out is a critical mechanism that allows the long-term persistence of saplings of these species in this winter deciduous forest. Studies and models of C gain, growth, and survival of saplings in deciduous forests may need to take into account their spring phenology because saplings of many species are actually "sun" individuals in the spring prior to their longer period in the summer shade.