Small mammal personalities generate context dependence in the seed dispersal mutualism.

Mutualisms are foundational components of ecosystems with the capacity to generate biodiversity through adaptation and coevolution and give rise to essential services such as pollination and seed dispersal. To understand how mutualistic interactions shape communities and ecosystems, we must identify the mechanisms that underlie their functioning. One mechanism that may drive mutualisms to vary in space and time is the unique behavioral types, or personalities, of the individuals involved. Here, our goal was to examine interindividual variation in the seed dispersal mutualism and identify the role that different personalities play. In a field experiment, we observed individual deer mice (Peromyscus maniculatus) with known personality traits predating and dispersing seeds in a natural environment and classified all observed interactions made by individuals as either positive or negative. We then scored mice on a continuum from antagonistic to mutualistic and found that within a population of scatter hoarders, some individuals are more mutualistic than others and that one factor driving this distinction is animal personality. Through this empirical work, we provide a conceptual advancement to the study of mutualism by integrating it with the study of intraspecific behavioral variation. These findings indicate that animal personality is a previously overlooked mechanism generating context dependence in plant­animal interactions and suggest that behavioral diversity may have important consequences for the functioning of mutualisms.

Natural selection on floral volatiles and other traits can change with snowmelt timing and summer precipitation.

Climate change is disrupting floral traits that mediate mutualistic and antagonistic species interactions. Plastic responses of these traits to multiple shifting conditions may be adaptive, depending on natural selection in new environments. We manipulated snowmelt date over three seasons (3-11 d earlier) in factorial combination with growing-season precipitation (normal, halved, or doubled) to measure plastic responses of volatile emissions and other floral traits in Ipomopsis aggregata. We quantified how precipitation and early snowmelt affected selection on traits by seed predators and pollinators. Within years, floral emissions did not respond to precipitation treatments but shifted with snowmelt treatment depending on the year. Across 3 yr, emissions correlated with both precipitation and snowmelt date. These effects were driven by changes in soil moisture. Selection on several traits changed with earlier snowmelt or reduced precipitation, in some cases driven by predispersal seed predation. Floral trait plasticity was not generally adaptive. Floral volatile emissions shifted in the face of two effects of climate change, and the new environments modulated selection imposed by interacting species. The complexity of the responses underscores the need for more studies of how climate change will affect floral volatiles and other floral traits.

Offspring may succeed well next to their relatives, but it needs particular traits.

BACKGROUND AND AIMS: There is ongoing debate about whether offspring perform best next to phylogenetically distantly related adult neighbours (due to the scarcity of enemies and competitors) or next to closely related adults (due to the abundance of mutualists). Here we hypothesise that relatedness of adult neighbours affects which traits confer performance rather than performance itself. METHODS: We studied seed removal, seed germination and sapling growth in Sessile Oaks (Quercus petraea and hybrids), and how they depend on size, shape and other traits, under both closely and distantly related canopies, manipulating offspring-density, presence of insects, and fungi, and spatial proximity to oaks. KEY RESULTS: We found that phylogenetic distance of adult neighbours affects only little performance of offspring but strongly which traits confer performance to offspring, in particular the size and shape of seeds and saplings. Differences in trait-performance relationships mostly disappear once insects or conspecific competitors are excluded (albeit exclusion of fungi reinforced these differences). Effects of phylogenetic distance of neighbours were not replaceable by the percentage of the gymnosperms among neighbours, nor the environmental conditions considered. CONCLUSIONS: We suggest that by responding to a biotic micro-mosaic of selection pressures, Sessile Oak flexibly succeeds in diverse neighbourhoods. Sessile Oak might maintain the potential for both, convergence with and divergence from phylogenetically distantly related species, thereby reinforcing or eroding phylogenetic signal of niches.

The effect of local habitat and spatial connectivity on urban seed predation.

PREMISE: During the last centuries, the area covered by urban landscapes is increasing all over the world. Urbanization can change local habitats and decrease connectivity among these habitats, with important consequences for species interactions. While several studies have found a major imprint of urbanization on plant-insect interactions, the effects of urbanization on seed predation remain largely unexplored. METHODS: We investigated the relative impact of sunlight exposure, leaf litter, and spatial connectivity on predation by moth and weevil larvae on acorns of the pedunculate oak across an urban landscape during 2018 and 2020. We also examined whether infestations by moths and weevils were independent of each other. RESULTS: While seed predation varied strongly among trees, seed predation was not related to differences in sunlight exposure, leaf litter, or spatial connectivity. Seed predation by moths and weevils was negatively correlated at the level of individual acorns in 2018, but positively correlated at the acorn and the tree level in 2020. CONCLUSIONS: Our study sets the baseline expectation that urban seed predators are unaffected by differences in sunlight exposure, leaf litter, and spatial connectivity. Overall, our findings suggest that the impact of local and spatial factors on insects within an urban context may depend on the species guild. Understanding the impact of local and spatial factors on biodiversity, food web structure, and ecosystem functioning can provide valuable insights for urban planning and management strategies aimed at promoting urban insect diversity.

Natural and anthropogenic factors influence flowering synchrony and reproduction of a dominant plant in an inter-Andean scrub.

PREMISE: Agriculture expansion, livestock, and global change have transformed biological communities and altered, through aerosols and direct deposition, N:P balance in soils of inter-Andean valleys, potentially affecting flowering phenology of many species and thereby flowering synchrony and plant reproduction. METHODS: We evaluated the influence of variation in temperature and moisture along the local elevational gradient and treatments with the addition of N and P and grazing on flowering synchrony and reproduction of Croton, a dominant shrub of the inter-Andean dry scrub. Along the elevational gradient (300 m difference between the lowest and highest site), we set up plots with and without grazing nested with four nutrient treatments: control and addition of N or P alone or combined N + P. We recorded the number of female and male flowers in bloom monthly from September 2017 to August 2019 to calculate flowering synchrony. We assessed fruiting, seed mass, and pre-dispersal seed predation. RESULTS: Higher growing-season soil temperatures, which were negatively associated with local elevation and higher nitrogen availability promoted flowering synchrony of Croton, particularly among larger plants. Greater flowering synchrony, high soil temperatures, and addition of N + P resulted in production of more fruits of Croton, but also intensified pre-dispersal seed predation. CONCLUSIONS: Temperature, availability of moisture throughout the elevational gradient, and nutrient manipulation affected flowering synchrony, which subsequently affected production of fruits in Croton. These results emphasize the critical role of current anthropogenic changes in climate and nutrient availability on flowering synchrony and reproduction of Croton, a dominant plant of the inter-Andean scrub.

Flower position within plants influences reproductive success both directly and via phenology.

PREMISE: In plants, within-individual trait variation might result from mechanisms related to ontogenetic contingency, i.e., to the position of a particular structure within the plant, previous developmental events, and/or the developmental environment. Flower position within inflorescences as well as inflorescence position within plants can influence resource provisioning, phenology, biotic interactions, and reproductive success. Despite the potential implications of within-individual variation in plant reproductive phenotypes, its causes and effects on reproductive success are still little explored. METHODS: We assessed how reproductive success, in terms of fruit and seed set, and seed predation of 5883 flowers in Lathyrus vernus were influenced by their position within and among racemes, to what extent relationships between flower position and reproductive success and seed predation were mediated by phenology, and if positional effects on reproductive success depended on the external environment. RESULTS: In three years, basal flowers and racemes opened earlier and had higher fruit set than distal. Basal flowers also experienced higher seed predation. Differences among racemes in fruit and seed set were largely related to phenology, while differences in fruit set, seed set, and seed predation within racemes were not. In one year, differences in fruit set among flowers at different positions depended on flowering duration. CONCLUSIONS: Our results highlight the important role of ontogenetic contingency for within-individual variation in phenology and reproductive success. As the spatial distribution of reproductive structures affects both within-plant trait distributions and fitness, it is a likely target for natural selection.

Ground beetle movement is deterred by habitat edges: a mark-release-recapture study on the effectiveness of border crops in an agricultural landscape.

Border crops can increase beneficial insect biodiversity within agricultural fields by supplementing insects with food and nesting resources. However, the effectiveness of border crops relies on insect movement between adjacent habitats and some insects might consider habitat boundaries as barriers. Therefore, understanding insect movement between habitats is needed to determine the effectiveness of border crops for ecosystem services such as pest control within agricultural habitats. Our objective was to compare ground beetle (Coleoptera: Carabidae) movement across soybean plots that were bordered by corn and grassland habitat to determine whether habitat boundaries were considered barriers of movement to predatory beetles. Using a grid of pitfall traps within these habitats, we conducted a mark, release, and recapture experiment to track and evaluate ground beetle movement patterns. We found that ground beetles stayed in the habitat of their release and that movement between habitats, despite the type of bordering habitat or type of edge, was uncommon. We also found that long-distance movement was rare as most beetles moved less than 5 m (regardless of release or recaptured habitat) and movement was perpendicular to habitat edges. These results suggest that any edge habitat, including agricultural-agricultural boundaries and natural-agricultural boundaries, are likely barriers to ground beetle movement. Therefore, in order for border crops to be effective in pest management by ground beetles, making habitat edges more permeable, especially using techniques such as edge softening, could promote cross-habitat movement and ultimately contribute to natural pest control in agricultural systems.

Reproductive collapse in European beech results from declining pollination efficiency in large trees.

Climate warming increases tree mortality which will require sufficient reproduction to ensure population viability. However, the response of tree reproduction to climate change remains poorly understood. Warming can reduce synchrony and interannual variability of seed production ("masting breakdown") which can increase seed predation and decrease pollination efficiency in trees. Here, using 40 years of observations of individual seed production in European beech (Fagus sylvatica), we showed that masting breakdown results in declining viable seed production over time, in contrast to the positive trend apparent in raw seed count data. Furthermore, tree size modulates the consequences of masting breakdown on viable seed production. While seed predation increased over time mainly in small trees, pollination efficiency disproportionately decreased in larger individuals. Consequently, fecundity declined over time across all size classes, but the overall effect was greatest in large trees. Our study showed that a fundamental biological relationship-correlation between tree size and viable seed production-has been reversed as the climate has warmed. That reversal has diverse consequences for forest dynamics; including for stand- and biogeographical-level dynamics of forest regeneration. The tree size effects suggest management options to increase forest resilience under changing climates.

Effects of experimental warming on floral scent, display, and rewards in two subalpine herbs.

BACKGROUND AND AIMS: Floral volatiles, visual traits, and rewards mediate attraction and defense in plant-pollinator and plant-herbivore interactions, but these floral traits may be altered by global warming through direct effects of temperature or longer term impacts on plant resources. We examined the effect of warming on floral and leaf volatile emissions, floral morphology, plant height, nectar production, and oviposition by seed predators. METHODS: We used open-top chambers that warmed plants in the field +2-3 °C on average (+6-11 °C increase in daily maxima) for 2-4 weeks across 1-3 years at 3 sites in Colorado, USA. Volatiles were sampled from two closely related species of subalpine Ipomopsis with different pollinators: I. aggregata ssp. aggregata, visited mainly by hummingbirds, and I. tenuituba ssp. tenuituba, often visited by hawkmoths. KEY RESULTS: While warming had no detected effects on leaf volatiles, the daytime floral volatiles of both I. aggregata and I. tenuituba responded in subtle ways to warming, with impacts that depended on the species, site, and year. In addition to the long-term effect of warming, temperature at the time of sampling independently affected the floral volatile emissions of I. aggregata during the day and I. tenuituba at night. Warming had little effect on floral morphology for either species, and no effect on nectar concentration, maximum inflorescence height, or flower redness in I. aggregata. However, warming increased nectar production in I. aggregata by 41%, a response that would attract more hummingbird visits, and reduced oviposition by fly seed predators by at least 72%. CONCLUSIONS: Our results suggest that floral traits can show different levels of plasticity to temperature changes in subalpine environments, with potential effects on animal behaviors that help or hinder plant reproduction. They also illustrate the need for more long-term field warming studies, as shown by responses of floral volatiles in different ways to weeks of warming versus temperature at the time of sampling.

Contrasting seed traits of co-existing seeds lead to a complex neighbor effect in a seed-rodent interaction.

Scatter-hoarding rodents play important roles in seed dispersal and predation in many forest ecosystems. Existing studies have shown that the seed foraging preference of rodents is directly affected by seed traits and indirectly affected by the traits of other co-existing seeds nearby (i.e., neighbor effect). Plant seeds exhibit a combination of diverse seed traits, including seed size, chemical defense, and nutrient content. Therefore, it is difficult to evaluate the influence of each single seed trait on such neighbor effects. Here, by using artificial seeds, we investigated the impacts of contrasts in seed size, tannin content, and nutrient content on neighbor effects. We tracked 9000 tagged artificial seeds from 30 seed-seed paired treatments in a subtropical forest in southwest China. The contrast in seed size between paired seeds created obvious neighbor effects measured through three seed dispersal related indicators: the proportion of seeds being removed, the proportion of seeds cached, and the distance transported by rodents. However, the magnitudes and the signs of the neighbor effects differed among pairs, including both apparent mutualism and apparent competition, depending on the contrast in seed size between paired seeds. The contrasts of tannin and nutrient content between paired seeds showed relatively few neighbor effects. Our results suggest that the contrast in seed traits between the target seed and its neighboring seeds should be considered when studying rodent-seed interactions. Furthermore, we expect that similar complex neighbor effects may also exist in other plant-animal interactions, such as pollination and herbivory.

Sympatric primate seed dispersers and predators jointly contribute to plant diversity in a subtropical forest.

Mutualistic and antagonistic plant-animal interactions differentially contribute to the maintenance of species diversity in ecological communities. Although both seed dispersal and predation by fruit-eating animals are recognized as important drivers of plant population dynamics, the mechanisms underlying how seed dispersers and predators jointly affect plant diversity remain largely unexplored. Based on mediating roles of seed size and species abundance, we investigated the effects of seed dispersal and predation by two sympatric primates (Nomascus concolor and Trachypithecus crepusculus) on local plant recruitment in a subtropical forest of China. Over a 26 month period, we confirmed that these primates were functionally distinct: gibbons were legitimate seed dispersers who dispersed seeds of 44 plant species, while langurs were primarily seed predators who destroyed seeds of 48 plant species. Gibbons dispersed medium-seeded species more effectively than small- and large-seeded species, and dispersed more seeds of rare species than common and dominant species. Langurs showed a similar predation rate across different sizes of seeds, but destroyed a large number of seeds from common species. Due to gut passage effects, gibbons significantly shortened the duration of seed germination for 58% of the dispersed species; however, for 54% of species, seed germination rates were reduced significantly. Our study underlined the contrasting contributions of two primate species to local plant recruitment processes. By dispersing rare species and destroying the seeds of common species, both primates might jointly maintain plant species diversity. To maintain healthy ecosystems, the conservation of mammals that play critical functional roles needs to receive further attention.

Emerging infectious disease triggered a trophic cascade and enhanced recruitment of a masting tree.

There are several mechanisms that allow plants to temporarily escape from top-down control. One of them is trophic cascades triggered by top predators or pathogens. Another is satiation of consumers by mast seeding. These two mechanisms have traditionally been studied in separation. However, their combined action may have a greater effect on plant release than either process alone. In 2015, an outbreak of a disease (African swine fever, ASF) caused a crash in wild boar (Sus scrofa) abundance in Bialowieza Primeval Forest. Wild boar are important consumers of acorns and are difficult to satiate relative to less mobile granivores. We hypothesized that the joint action of the ASF outbreak and masting would enhance regeneration of oaks (Quercus robur). Data from ungulate exclosures demonstrated that ASF led to reduction in acorn predation. Tree seedling data indicated that oak recruitment increased twofold relative to pre-epidemic period. Our results showed that perturbations caused by wildlife disease travel through food webs and influence forest dynamics. The outbreak of ASF acted synergistically with masting and removed herbivore top-down control of oaks by mobile consumers. This illustrates that the ASF epidemic that currently occurs across Europe can have broad effects on forest dynamics.

Costs and benefits of masting: economies of scale are not reduced by negative density-dependence in seedling survival in Sorbus aucuparia.

Masting is a widespread reproductive strategy in plants that helps to reduce seed predation and increase pollination. However, masting can involve costs, notably negative density-dependent (NDD) seedling survival caused by concentrating reproduction in intermittent events. Masting benefits have received widespread attention, but the costs are understudied, which precludes understanding why some plant species have evolved intense masting, while others reproduce regularly. We followed seed production, seed predation (both 13 yr), and seedling recruitment and survival (11 yr) in Sorbus aucuparia. We tested whether NDD in seedling survival after mast years can reduce the benefits of pulsed reproduction that come through predator satiation. Seed predation rates were extreme in our population (mean = 75%), but were reduced by masting. The commonly accepted, but untested, assertion that pulsed recruitment is associated with strong NDD was unsupported. Consequently, the proportion of seedlings that survived their first year increased with fruit production. This provides a rare test of economies of scale beyond the seed stage. Our results provide estimation of the costs of mast seeding, and indicate that these may be lower than expected. Low masting costs, if common, may help explain why masting is such a widespread reproductive strategy throughout the plant kingdom.

Seed size-seed number trade-offs: influence of seed size on the density of fire-stimulated persistent soil seed banks.

PREMISE: Does the seed size-seed number allocation trade-off model apply to long-term persistent soil seed banks? This trade-off between seed size versus number of seeds produced is usually applied at a single population on an annual basis. Our question is how this model might apply to close relatives that produce dormant seed forming long-term persistent soil seed banks. These two criteria allow a focus on divergent evolution of conspecifics and permits us to isolate seed size in the spectrum of life history traits that may be influencing seed traits, and on how seed size influences accumulation and persistence in the soil. METHODS: In California, Arctostaphylos species only produce physiologically dormant seed that are fire-stimulated and that vary in seed size permitting seed size-seed bank density relationship as a test of the seed size-seed number allocation model. Soil seed banks of 10 species of Arctostaphylos were sampled with fruit volumes ranging from 21-1063 mm3 . Seed bank density was determined by hand extraction from soil samples. RESULTS: We found that seed bank densities were significantly negatively related to fruit or seed size. CONCLUSIONS: Rather than an issue of allocational trade-off between size and number, we interpret these results as reflecting seed predation and postfire seedling establishment. Seed bank densities, even after decades, generally were less than one or two-year's seed production, suggesting intense seed predation. Burial by scatter-hoarding rodents provided sufficient seeds deep enough for survival of fire. Variation on seed size suggests seedling establishment constraints, but it needs further research.

The potential for floral evolution in response to competing selection pressures following the loss of hawkmoth pollination in Ruellia humilis.

PREMISE: In the absence of hawkmoth pollinators, chasmogamous (CH) flowers of Ruellia humilis self-pollinate by two secondary mechanisms. Other floral visitors might exert selection on CH floral traits to restore outcrossing, but at the same time preferential predation of CH seeds generates selection to increase the allocation of resources to cleistogamous (CL) flowers. METHODS: To assess the potential for an evolutionary response to these competing selection pressures, we estimated additive genetic variances ( σ A 2 ${\sigma }_{{\rm{A}}}^{2}$ ) and covariances for 14 reproductive traits and three fitness components in a Missouri population lacking hawkmoth pollinators. RESULTS: We found significant σ A 2 ${\sigma }_{{\rm{A}}}^{2}$ for all 11 floral traits and two measures of resource allocation to CL flowers, indicating the potential for a short-term response to selection on most reproductive traits. Selection generated by seed predators is predicted to increase the percentage of CL flowers by 0.24% per generation, and mean stigma-anther separation is predicted to decrease as a correlated response, increasing the fraction of plants that engage in prior selfing. However, the initial response to this selection is opposed by strong directional dominance. CONCLUSIONS: The predicted evolutionary decrease in the number of CH flowers available for potential outcrossing, combined with the apparent preclusion of potential diurnal pollinators by the pollen-harvesting activities of sweat bees, suggest that 100% cleistogamy is the likely outcome of evolution in the absence of hawkmoths. However, rare mutations with large effects, such as delaying budbreak until after sunrise, could provide pathways for the restoration of outcrossing that are not reachable by gradual quantitative-genetic evolution.

Seed predator effects on plants: Moving beyond time-corrected proxies.

We previously demonstrated that small mammals impact plant recruitment globally via size-dependent seed predation, generating a unimodal pattern across ecosystems. Chen et al. (2021) critiqued our seed removal analysis, advocating corrections for exposure time. We show such manipulations are unwarranted and argue for increased emphasis on plant recruitment metrics.

Exposure time is an important variable in quantifying post-dispersal seed removal.

A literature synthesis concluded that small mammals have the greatest impact on post-dispersal removal of intermediate-sized seeds (Dylewski et al. 2020). However, this study failed to consider the duration of seed exposure to predators. Re-analyses of the corrected dataset revealed only a weak effect of seed mass on seed removal.

When do Janzen-Connell effects matter? A phylogenetic meta-analysis of conspecific negative distance and density dependence experiments.

The Janzen-Connell (J-C) hypothesis suggests that specialised natural enemies cause distance- or density-dependent mortality among host plants and is regarded as an important mechanism for species coexistence. However, there remains debate about whether this phenomenon is widespread and how variation is structured across taxa and life stages. We performed the largest meta-analysis of experimental studies conducted under natural settings to date. We found little evidence of distance-dependent or density-dependent mortality when grouping all types of manipulations. Our analysis also reveals very large variation in response among species, with 38.5% of species even showing positive responses to manipulations. However, we found a strong signal of distance-dependent mortality among seedlings but not seed experiments, which we attribute to (a) seedlings sharing susceptible tissues with adults (leaves, wood, roots), (b) seedling enemies having worse dispersal than seed enemies and (c) seedlings having fewer physical and chemical defences than seeds. Both density- and distance-dependent mortality showed large variation within genera and families, suggesting that J-C effects are not strongly phylogenetically conserved. There were no clear trends with latitude, rainfall or study duration. We conclude that J-C effects may not be as pervasive as widely thought. Understanding the variation in J-C effects provides opportunities for new discoveries that will refine our understanding of J-C effects and its role in species coexistence.

Seed predation selects for reproductive variability and synchrony in perennial plants.

Annually variable and synchronous seed production by plant populations, or masting, is a widespread reproductive strategy in long-lived plants. Masting is thought to be selectively beneficial because interannual variability and synchrony increase the fitness of plants through economies of scale that decrease the cost of reproduction per surviving offspring. Predator satiation is believed to be a key economy of scale, but whether it can drive phenotypic evolution for masting in plants has been rarely explored. We used data from seven plant species (Quercus humilis, Quercus ilex, Quercus rubra, Quercus alba, Quercus montana, Sorbus aucuparia and Pinus pinea) to determine whether predispersal seed predation selects for plant phenotypes that mast. Predation selected for interannual variability in Mediterranean oaks (Q. humilis and Q. ilex), for synchrony in Q. rubra, and for both interannual variability and reproductive synchrony in S. aucuparia and P. pinea. Predation never selected for negative temporal autocorrelation of seed production. Predation by invertebrates appears to select for only some aspects of masting, most importantly high coefficient of variation, supporting individual-level benefits of the population-level phenomenon of mast seeding. Determining the selective benefits of masting is complex because of interactions with other seed predators, which may impose contradictory selective pressures.

Inconsistent annual compensation for floral herbivory by an iterocarpic thistle.

PREMISE: Plants experiencing steep reproductive losses from herbivores should favor strategies promoting tolerance or resistance to that herbivory. However, the degree to which such strategies succeed in improving plant fitness under natural conditions needs further evaluation, especially for iterocarpic species. We tested whether reproductive effort by the iterocarpic Cirsium undulatum Spreng. (Wavyleaf thistle) provided within-season tolerance for floral herbivory through response to apical damage. METHODS: We imposed apical damage and manipulated floral herbivory on later-flowering, non-apical flowerheads for two seasons. We asked: (1) is there evidence of compensatory potential to tolerate apical flowerhead damage? If so, (2) does the amount of herbivore pressure on non-apical flowerheads influence the magnitude of any compensatory response; and (3) is the response to apical damage sufficient to increase plant seed production under ambient floral herbivory over the flowering season? RESULTS: Plants showed compensatory potential for apical head loss; apical damage increased seed contributions from later, lower positioned flowerheads. Further, the intensity of subsequent herbivore pressure influenced compensation outcomes. Equitable seed production under both levels of ambient herbivory occurred only in the year in which plants were larger and insect pressure was lower. Finally, the response to apical damage was sufficient to compensate for apical seed loss, but it did not consistently increase overall annual seed production under ambient floral herbivory. CONCLUSIONS: Although this iterocarpic species can compensate for apical damage, tolerance for floral herbivory varied between years.