Nathanael I. Lichti

Seed fate and decision-making processes in scatter-hoarding rodents

A mechanistic understanding of seed movement and survival is important both for the development of theoretical models of plant population dynamics, spatial spread, and community assembly, and for the conservation and management of plant communities under global change. While models of wind‐borne seed dispersal have advanced rapidly over the past two decades, models for animal‐mediated dispersal have failed to make similar progress due to their dependence on interspecific interactions and complex, context‐dependent behaviours. In this review, we synthesize the literature on seed dispersal and consumption by scatter‐hoarding, granivorous rodents and outline a strategy for development of a general mechanistic seed‐fate model in these systems. Our review decomposes seed dispersal and survival into six distinct sub‐processes (exposure, harvest, allocation, preparation, placement, and recovery), and identifies nine intermediate (latent) variables that link physical state variables (e.g. seed and animal traits, habitat structure) to decisions regarding seed allocation to hoarding or consumption, cache placement and management, and deployment of radicle‐pruning or embryo excision behaviours. We also highlight specific areas where research on these intermediate relationships is needed to improve our mechanistic understanding of scatter‐hoarder behaviour. Finally, we outline a strategy to combine detailed studies on individual functional relationships with seed‐tracking experiments in an iterative, hierarchical Bayesian framework to construct, refine, and test mechanistic models for context‐dependent, scatter‐hoarder‐mediated seed fate.

Estimating utilization distributions with kernel versus local convex hull methods

ABSTRACT Estimates of utilization distributions (UDs) are used in analyses of home-range area, habitat and resource selection, and social interactions. We simulated data from 12 parent UDs, representing 3 series of increasingly intense space-use patterns (clustering of points around a home site, restriction of locations to a network of nodes and corridors, and dominance of a central hole in the UD) and compared the ability of kernel density estimation (KDE) and local convex hull (LCH) construction to reconstruct known UDs from samples of 10, 50, 250, and 1,000 location points. For KDE, we considered 4 bandwidth selectors: the reference bandwidth, least-squares cross-validation (LSCV), direct plug-in (DPI), and solve-the-equation (STE). For the sample sizes and UD patterns tested here, KDE achieved significantly higher volume-of-intersection (VI) scores with known parent UDs than did LCH; KDE also provided less biased home-range area estimates under many conditions. However, LCH minimized the UD volume that occurred outside the true home range boundary (Vout). Among the KDE bandwidth estimators, relative performance depended on the type and intensity of space use patterns, sample size, and the metric used to evaluate performance. Biologists should use KDE for UD and home range estimation within a probabilistic context, unless their objective is to exclude potentially unused areas by defining the area delimited by data.

Segregating the effects of seed traits and common ancestry of hardwood trees on eastern gray squirrel foraging decisions

The evolution of specific seed traits in scatter-hoarded tree species often has been attributed to granivore foraging behavior. However, the degree to which foraging investments and seed traits correlate with phylogenetic relationships among trees remains unexplored. We presented seeds of 23 different hardwood tree species (families Betulaceae, Fagaceae, Juglandaceae) to eastern gray squirrels (Sciurus carolinensis), and measured the time and distance travelled by squirrels that consumed or cached each seed. We estimated 11 physical and chemical seed traits for each species, and the phylogenetic relationships between the 23 hardwood trees. Variance partitioning revealed that considerable variation in foraging investment was attributable to seed traits alone (27–73%), and combined effects of seed traits and phylogeny of hardwood trees (5–55%). A phylogenetic PCA (pPCA) on seed traits and tree phylogeny resulted in 2 “global” axes of traits that were phylogenetically autocorrelated at the family and genus level and a third “local” axis in which traits were not phylogenetically autocorrelated. Collectively, these axes explained 30–76% of the variation in squirrel foraging investments. The first global pPCA axis, which produced large scores for seed species with thin shells, low lipid and high carbohydrate content, was negatively related to time to consume and cache seeds and travel distance to cache. The second global pPCA axis, which produced large scores for seeds with high protein, low tannin and low dormancy levels, was an important predictor of consumption time only. The local pPCA axis primarily reflected kernel mass. Although it explained only 12% of the variation in trait space and was not autocorrelated among phylogenetic clades, the local axis was related to all four squirrel foraging investments. Squirrel foraging behaviors are influenced by a combination of phylogenetically conserved and more evolutionarily labile seed traits that is consistent with a weak or more diffuse coevolutionary relationship between rodents and hardwood trees rather than a direct coevolutionary relationship.

Acorn-Foraging Preferences of Four Species of Free-Ranging Avian Seed Predators in Eastern Deciduous Forests

Abstract. Oaks (Quercus spp.) rely on vertebrates for seed dispersal. However, the extent to which dispersal is facilitated depends on the vertebrate species involved, its preferences for acorns of different species, and the relative availability of acorns. We examined foraging preferences by free-ranging individuals of four species of birds for acorns of white (Q. alba), black (Q. velutina), and pin (Q. palustris) oak. We photographed selection of acorns at feeding platforms and used discrete-choice models to estimate preferences. Blue Jays (Cyanocitta cristata) had strong and consistent preferences in the order pin oak > black oak > white oak, whereas Red-bellied Woodpeckers (Melanerpes carolinus) exhibited the same but weaker preferences. On the basis of acorns chemical and physical attributes, these birds appear to focus on maximizing the net value of cached food. Tufted Titmice (Baeolophus bicolor) and White-breasted Nuthatches (Sitta carolinensis) preferred acorns of both pin and white oak over those of black oak. These smaller birds may be limited in their ability to crack harder shells. Our analysis also suggests that competition for limited food resources can lead to instances in which the dominant food item selected is not the most preferred. Ecological studies of oak dispersal and recruitment should consider the role of food preferences by avian assemblages in conjunction with spatial and temporal variation in acorn availability.

Vegetative and Adaptive Traits Predict Different Outcomes for Restoration Using Hybrids

Hybridization has been implicated as a driver of speciation, extinction, and invasiveness, but can also provide resistant breeding stock following epidemics. However, evaluating the appropriateness of hybrids for use in restoration programs is difficult. Past the F1 generation, the proportion of a progenitor’s genome can vary widely, as can the combinations of parental genomes. Detailed genetic analysis can reveal this information, but cannot expose phenotypic alterations due to heterosis, transgressive traits, or changes in metabolism or development. In addition, because evolution is often driven by extreme individuals, decisions based on phenotypic averages of hybrid classes may have unintended results. We demonstrate a strategy to evaluate hybrids for use in restoration by visualizing hybrid phenotypes across selected groups of traits relative to both progenitor species. Specifically, we used discriminant analysis to differentiate among butternut (Juglans cinerea L.), black walnut (J. nigra L.), and Japanese walnut (J. ailantifolia Carr. var. cordiformis) using vegetative characters and then with functional adaptive traits associated with seedling performance. When projected onto the progenitor trait space, naturally occurring hybrids (J. × bixbyi Rehd.) between butternut and Japanese walnut showed introgression toward Japanese walnut at vegetative characters but exhibited a hybrid swarm at functional traits. Both results indicate that hybrids have morphological and ecological phenotypes that distinguish them from butternut, demonstrating a lack of ecological equivalency that should not be carried into restoration breeding efforts. Despite these discrepancies, some hybrids were projected into the space occupied by butternut seedlings’ 95% confidence ellipse, signifying that some hybrids were similar at the measured traits. Determining how to consistently identify these individuals is imperative for future breeding and species restoration efforts involving hybrids. Discriminant analysis provides a useful technique to visualize past selection mechanisms and current variation in hybrid populations, especially when key ecological traits that distinguish progenitors are unknown. Furthermore, discriminant analysis affords a tool to assess ecological equivalency of hybrid populations and breeding program efforts to select for certain traits and monitor the amount of variability of those traits, relative to progenitors.

Does multiple seed loading in Blue Jays result in selective dispersal of smaller acorns

Studies from both tropical and temperate systems show that scatter-hoarding rodents selectively disperse larger seeds farther from their source than smaller seeds, potentially increasing seedling establishment in larger-seeded plants. Size-biased dispersal is evident in many oaks (Quercus) and is true both across and within species. Here, we predict that intraspecifc variation in seed size also influences acorn dispersal by the Blue Jay (Cyanocitta cristata Linnaeus), but in an opposite manner. Blue Jays are gape-limited and selectively disperse smaller acorn species (e.g. pin oaks [Quercus palustris Münchh]), but often carry several acorns in their crop during a single dispersal event. We predict that jays foraging on smaller acorns will load more seeds per trip and disperse seeds to greater distances than when single acorns are carried in the bill. To test this, we presented free-ranging Blue Jays with pin oak acorns of different sizes over a 2-year period. In each of 16 experimental trials, we monitored the birds at a feeding station with remote cameras and determined the number of acorns removed and the distance acorns were dispersed when cached. Jays were significantly more likely to engage in multiple seed loading with smaller seeds in both years of the study. During the second year, these smaller acorns were dispersed farther than larger acorns, and during the first year, larger acorns were dispersed farther, revealing an inconsistent response to seed size during our study. We suggest that in some circumstances, multiple seed loading by Blue Jays may favor dispersal in some plant species.

Selection ratios on community aggregated traits estimate ecological filters imposed on species by sites

Variation in community structure is mediated by interactions between species traits and a sites environmental characteristics. Previously, data on community composition at sites has been employed to correlate trait and environmental variables (e.g., RLQ analysis) and to predict community-level expression of quantitative traits (i.e., community aggregated traits). Here, we demonstrate that the selection ratio, a method originating in animal resource selection studies, can estimate the ecological filters that site conditions impose on species traits by combining observed community aggregated traits with null models of species availability. This flexible, nonparametric approach expresses the filter at each site as a probability density function for the selection of individuals possessing a given trait value. By doing so, it generalizes the community aggregated trait concept to include categorical as well as continuous traits and allows for both intraspecific variation in trait expression and differences in species availability among sites. The resulting site-level filter functions can be related to environmental covariates by standard statistical approaches (e.g., regression). The method complements existing techniques for analyzing trait-environment interactions in community ecology.

Eastern gray squirrels are consistent shoppers of seed traits: insights from discrete choice experiments

Seeds of many hardwood trees are dispersed by scatter-hoarding rodents, and this process is often mediated by the traits of seeds. Although numerous studies have linked seed traits to seed preference by rodents, little is known about how rodents forage for seeds when multiple desirable and undesirable seed traits are available simultaneously. Here, we adopt a novel method of designing choice experiments to study how eastern gray squirrels (Sciurus carolinensis) select for 6 traits (caloric value, protein content, tannin concentration, kernel mass, dormancy period and toughness of shell) among seeds. From n = 426 seed-pair presentations, we found that squirrels preferentially consumed seeds with short dormancy or tougher shells, and preferentially cached seeds with larger kernel mass, tougher shells and higher tannin concentrations. By incorporating random effects, we found that squirrels exhibited consistent preferences for seed traits, which is likely due to the fitness consequences associated with maintaining cached resources. Furthermore, we found that squirrels were willing to trade between multiple traits when caching seeds, which likely results in more seed species being cached in the fall. Ultimately, our approach allowed us to compute the relative values of different seed traits to squirrels, despite covariance among studied traits across seed species. In addition, by investigating how squirrels trade among different seed traits, important insights can be gleaned into behavioral mechanisms underlying seed caching (and, thus, seed survival) dynamics as well as evolutionary strategies adopted by plants to attract seed dispersers. We describe how discrete choice experiments can be used to study resource selection in other ecological systems.

Scatterhoarders drive long‐ and short‐term population dynamics of a nut‐producing tree, while pre‐dispersal seed predators and herbivores have little effect

Summary 1.Both seed predators and herbivores can have profound effects on individual plant growth, reproduction and survival, but their population level effects are less well understood. While most plants interact with a suite of seed predators and herbivores over their life cycle, few studies incorporate the effects of multiple interacting partners and multiple life stages on plant population growth. 2.We constructed a matrix model using six years of data from a rare, seed-producing population of American chestnut (Castanea dentata). We combined field demographic data with published experimental results on the effects of pre-dispersal seed predators (weevils) and post-dispersal seed predators (scatter-hoarding vertebrates) and incorporated the effect of vertebrate herbivores estimated from the field data. We explored the impact of these three different animal interactions for short-term (transient) and long-term (asymptotic) tree population growth. In addition, we used the model to explore the conditions under which scatter-hoarding would function as a mutualism. 3.Seed predators had greater effect on both short- and long-term population growth than herbivores. Although weevil infestation can greatly reduce the probability of germination, pre-dispersal seed predators had smaller effects on both short- or long-term population growth than post-dispersal predators. The elasticities of weevil-related parameters were also small. The effect of browsers on both the short- and long-term population growth rate were the smallest of the effects studied. Post-dispersal seed predation affected population growth the most of the interactions studied. The probability of seed removal was amongst the largest elasticities, similar in magnitude to survival of large trees. 4.Synthesis Our results indicate that neither weevils nor the intensity of browse damage observed at our study site are likely to hinder tree regeneration or reintroduction, though both reduced population growth. Although researchers and forest managers often assume that seeds are unimportant for long-lived tree populations, our test of this assumption shows that scatterhoarders and other post-dispersal seed consumers can significantly limit natural regeneration. Forest management that alters scatterhoarder behaviour could have significant effects on tree population dynamics that are largely unexplored. This article is protected by copyright. All rights reserved.

Forecasting effects of tree species reintroduction strategies on carbon stocks in a future without historical analog

American chestnut (Castanea dentata) was once an important component forests in the central Appalachians (USA), but it was functionally extirpated nearly a century ago. Attempts are underway to reintroduce blight-resistant chestnut to its former range, but it is uncertain how current forest composition, climate, and atmospheric changes and disturbance regimes will interact to determine future forest dynamics and ecosystem services. The combination of novel environmental conditions (e.g. climate change), a reintroduced tree species and new disturbance regimes (e.g. exotic insect pests, fire suppression) have no analog in the past that can be used to parameterize phenomenological models. We therefore used a mechanistic approach within the LANDIS-II forest landscape model that relies on physiological first principles to project forest dynamics as the outcome of competition of tree cohorts for light and water as a function of temperature, precipitation, CO2 concentration, and life history traits. We conducted a factorial landscape simulation experiment to evaluate specific hypotheses about future forest dynamics in two study sites in the center of the former range of chestnut. Our results supported the hypotheses that climate change would favor chestnut because of its optimal temperature range and relative drought resistance, and that chestnut would be less competitive in the more mesic Appalachian Plateau province because competitors will be less stressed. The hypothesis that chestnut will increase carbon stocks was supported, although the increase was modest. Our results confirm that aggressive restoration is needed regardless of climate and soils, and that increased aggressiveness of chestnut restoration increased biomass accumulation. The hypothesis that chestnut restoration will increase both compositional and structural richness was not supported because chestnut displaced some species and age cohorts. Although chestnut restoration did not markedly enhance carbon stocks, our findings provide hope that this formerly important species can be successfully reintroduced and associated ecosystem services recovered.