Global patterns in the predator satiation effect of masting: A meta-analysis.

SignificanceMasting, or synchronous production of large seed crops, is widespread among plants. The predator satiation hypothesis states that masting evolved to overwhelm seed predators with an excess of food. Yet, this popular explanation faced few rigorous tests. We conducted a meta-analysis of studies that related the magnitude of seed production to the intensity of seed predation. Our results validate certain theoretical notions (e.g., that predator satiation is more effective at higher latitudes) but challenge others (e.g., that specialist and generalist consumers differ in the type of functional response to masting). We also found that masting is losing its ability to satiate consumers, probably because global warming affected masting patterns. This shift might considerably impair the reproduction of masting plants.

Functional redundancy of weed seed predation is reduced by intensified agriculture.

Intensified agriculture, a driver of biodiversity loss, can diminish ecosystem functions and their stability. Biodiversity can increase functional redundancy and is expected to stabilize ecosystem functions. Few studies, however, have explored how agricultural intensity affects functional redundancy and its link with ecosystem function stability. Here, within a continental-wide study, we assess how functional redundancy of seed predation is affected by agricultural intensity and landscape simplification. By combining carabid abundances with molecular gut content data, functional redundancy of seed predation was quantified for 65 weed genera across 60 fields in four European countries. Across weed genera, functional redundancy was reduced with high field management intensity and simplified crop rotations. Moreover, functional redundancy increased the spatial stability of weed seed predation at the field scale. We found that ecosystem functions are vulnerable to disturbances in intensively managed agroecosystems, providing empirical evidence of the importance of biodiversity for stable ecosystem functions across space.

Predicting how defaunation-induced changes in seed predation and dispersal will affect tropical tree populations.

The loss of large animals due to overhunting and habitat loss potentially affects tropical tree populations and carbon cycling. Trees reliant on large-bodied seed dispersers are thought to be particularly negatively affected by defaunation. But besides seed dispersal, defaunation can also increase or decrease seed predation. It remains unclear how these different defaunation effects on early life stages ultimately affect tree population dynamics. We reviewed the literature on how tropical animal loss affects different plant life stages, and we conducted a meta-analysis of how defaunation affects seed predation. We used this information to parameterize models that altered matrix projection models from a suite of tree species to simulate defaunation-caused changes in seed dispersal and predation. We assessed how applying these defaunation effects affected population growth rates. On average, population-level effects of defaunation were negligible, suggesting that defaunation may not cause the massive reductions in forest carbon storage that have been predicted. In contrast to previous hypotheses, we did not detect an effect of seed size on changes in seed predation rates. The change in seed predation did not differ significantly between exclosure experiments and observational studies, although the results of observational studies were far more variable. Although defaunation surely affects certain tree taxa, species that benefit or are harmed by it and net changes in forest carbon storage cannot currently be predicted based on available data. Further research on how factors such as seed predation vary across tree species and defaunation scenarios is necessary for understanding cascading changes in species composition and diversity.

Predicciones de cómo los cambios inducidos en la dispersión y depredación de semillas por la pérdida de fauna afectará a las poblaciones de árboles tropicales Resumen La pérdida de animales grandes debido a la caza excesiva y la pérdida del hábitat afecta potencialmente a las poblaciones de árboles tropicales y al ciclo del carbono. Se considera que los árboles que dependen de dispersores de semillas de talla grande son los más afectados negativamente por la pérdida de fauna. La defaunación también puede incrementar o disminuir la depredación de semillas, además de su dispersión. Todavía no está claro cómo afectan al final a las dinámicas poblaciones de los árboles los diferentes efectos de la pérdida de fauna en las etapas temprana de vida. Revisamos la literatura sobre cómo la pérdida de animales tropicales afecta las diferentes etapas de vida de las plantas y realizamos un metaanálisis sobre cómo la pérdida de fauna afecta a la depredación de semillas. Usamos esta información para definir los parámetros de los modelos que alteraron los modelos de proyección de matriz a partir de un conjunto de especies de árboles y así simular los cambios causados por la pérdida de fauna en la dispersión y depredación de semillas. Analizamos cómo la aplicación de estos efectos de pérdida de fauna afectó las tasas de crecimiento poblacional. En promedio, los efectos de la pérdida de fauna a nivel poblacional fueron no significativas, lo que sugiere que la pérdida de fauna puede no ser la causa de las reducciones masivas que se han pronosticado en el almacenamiento de carbono forestal. Contrario a las hipótesis previas, no detectamos ningún efecto del tamaño de las semillas sobre los cambios en las tasas de depredación. El cambio en la depredación de semillas no difirió significativamente entre los experimentos de encierro y los estudios de observación, aunque los resultados de los últimos fueron mucho más variables. Mientras que la pérdida de fauna seguramente afecta a ciertos taxones de árboles, actualmente no se pueden pronosticar, con base en los datos disponibles, las especies que se benefician o perjudican por esta pérdida y los cambios netos en el almacenamiento de carbono forestal. Se necesita una investigación más avanzada sobre cómo varían los factores, como la depredación de semillas, entre especies de árboles y escenarios de pérdida de fauna para entender los cambios en cascada en la composición y diversidad de las especies.

Seed predation-induced Allee effects, seed dispersal and masting jointly drive the diversity of seed sources during population expansion.

The environmental factors affecting plant reproduction and effective dispersal, in particular biotic interactions, have a strong influence on plant expansion dynamics, but their demographic and genetic consequences remain an understudied body of theory. Here, we use a mathematical model in a one-dimensional space and on a single reproductive period to describe the joint effects of predispersal seed insect predators foraging strategy and plant reproduction strategy (masting) on the spatio-temporal dynamics of seed sources diversity in the colonisation front of expanding plant populations. We show that certain foraging strategies can result in a higher seed predation rate at the colonisation front compared to the core of the population, leading to an Allee effect. This effect promotes the contribution of seed sources from the core to the colonisation front, with long-distance dispersal further increasing this contribution. As a consequence, our study reveals a novel impact of the predispersal seed predation-induced Allee effect, which mitigates the erosion of diversity in expanding populations. We use rearrangement inequalities to show that masting has a buffering role: it mitigates this seed predation-induced Allee effect. This study shows that predispersal seed predation, plant reproductive strategies and seed dispersal patterns can be intermingled drivers of the diversity of seed sources in expanding plant populations, and opens new perspectives concerning the analysis of more complex models such as integro-difference or reaction-diffusion equations.

The functional form of specialised predation affects whether Janzen-Connell effects can prevent competitive exclusion.

Janzen-Connell effects (JCEs), specialised predation of seeds and seedlings near conspecific trees, are hypothesised to maintain species richness. While previous studies show JCEs can maintain high richness relative to neutral communities, recent theoretical work indicates JCEs may weakly inhibit competitive exclusion when species exhibit interspecific fitness variation. However, recent models make somewhat restrictive assumptions about the functional form of specialised predation-that JCEs occur at a fixed rate when offspring are within a fixed distance of a conspecific tree. Using a theoretical model, I show that the functional form of JCEs largely impacts their ability to maintain coexistence. If predation pressure increases additively with adult tree density and decays exponentially with distance, JCEs maintain considerably higher species richness than predicted by recent models. Loosely parameterising the model with data from a Panamanian tree community, I elucidate the conditions under which JCEs are capable of maintaining high species richness.

How will global change affect plant reproduction? A framework for mast seeding trends.

Forest ecology traditionally focuses on plant growth and survival, leaving seed production as a major demographic process lacking a framework for how it will be affected by global change. Understanding plant reproductive responses to changing climate is complicated by masting, the annually variable seed production synchronized within populations. Predicting trends in masting is crucial, because masting impacts seed predation and pollination enough to override simple trends in mean seed production. Proximate mechanisms of seed production patterns in perennial plants are gathered to identify processes through which masting may be affected by a changing environment. Predicting trends in masting will require understanding the mechanisms that cause predictable seed failure after high-seed years, and the stochastic mechanisms that synchronize individuals in high-seed years.

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.

The selective advantage of mast flowering in Veratrum album subsp. oxysepalum: Implications of the predator satiation hypothesis.

PREMISE: Synchronous, highly variable flower or seed production among years within a population (i.e., masting) has been reported in numerous perennial plants. Although masting provides ecological advantages such as enhancing pollination efficiency and/or escape from predator attack, little is known about the degree of these advantages and variations in masting behavior among populations of conspecific plants. METHODS: We determined flowering ramet density and reproductive success (fruit-set success and herbivorous damage) of a perennial herb, Veratrum album subsp. oxysepalum, across six lowland and six alpine populations in northern Japan during 2-3 years. We then analyzed the relationship between floral density and reproductive success to assess the ecological significance of mast flowering. Flowering intervals of individual plants were estimated by counting annual scars on rhizomes. RESULTS: Most populations had mast flowering, but the intervals between flowering for individual plants were shorter in the alpine populations than in the lowland populations. Floral damage by stem borers (dipteran larvae) and seed predation by lepidopteran larvae were intense in the lowland populations. Seed production of individual ramets increased with higher floral density owing to the effective avoidance of floral-stem damage and seed predation. Although stem borers were absent in the alpine habitat, seed predation decreased with higher floral density also in the alpine populations. Pollination success was independent of floral density in both of the alpine and lowland populations. CONCLUSIONS: These results strongly support the predator satiation hypothesis for mast flowering by this species.

Invasive grass indirectly alters seasonal patterns in seed predation.

Invasive species threaten ecosystems globally, but their impacts can be cryptic when they occur indirectly. Invader phenology can also differ from that of native species, potentially causing seasonality in invader impacts. Yet, it is unclear if invader phenology can drive seasonal patterns in indirect effects. We used a field experiment to test if an invasive grass (Imperata cylindrica) caused seasonal indirect effects by altering rodent foraging and seed predation patterns through time. Using seeds from native longleaf pine (Pinus palustris), we found seed predation was 25% greater, on average, in invaded than control plots, but this effect varied by season. Seed predation was 24-157% greater in invaded plots during spring and autumn months, but invasion had no effect on seed predation in other months. One of the largest effects occurred in October when longleaf pine seeds are dispersed, suggesting potential effects on tree regeneration. Thus, seasonal patterns in indirect effects from invaders may cause underappreciated impacts on ecological communities.

Seed and seedling predation by vertebrates mediates the effects of adult trees in two temperate tree species.

Specialised natural enemies can locally suppress seeds and seedlings near conspecific adults more than far from them. Whilst this is thought to facilitate species coexistence, the relative contribution of multiple enemies to whether heterospecific seeds and seedlings rather than conspecifics perform better beneath a particular adult species remains less clear, especially in regions with spatially extensive monodominant stands. We designed a field exclusion experiment to separate the effects of fungi, insects and vertebrates on the seedling establishment and early survival of two temperate tree species, Fagus sylvatica and Picea abies, in the adult tree monocultures of these species. Our experiment demonstrates the key role of vertebrates in mediating the effects of adult trees on seeds and seedlings. Due to vertebrates and partly insects, Fagus sylvatica seedlings survived worse beneath conspecific than heterospecific adults and were also outperformed by Picea abies seedlings beneath their own adults. Picea abies seedling establishment was higher beneath conspecific than heterospecific adults, but Fagus sylvatica seedlings outperformed them beneath their own adults. The impact of enemies on Picea abies establishment beneath conspecific adults was less clear. Fungi did not influence seedling establishment and survival. Our findings highlight the need to compare enemy impacts on each seedling species beneath conspecific and heterospecific adults with their impacts on conspecific and heterospecific seedlings beneath a particular adult species. Such evaluations can shed more light on the role of enemies in tree communities by identifying the plant-enemy interactions that facilitate species coexistence and those that promote species monodominance.

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.

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.

Pre-dispersal seed predators boost seed production in a short-lived plant.

Pre-dispersal seed predation diminishes fitness and population growth rate of many plant species. Therefore, plants have developed multiple strategies to reduce the harmful effects of this type of herbivory. The present study aims to determine the effect of pre-dispersal seed predators (PSPs) on the fitness of a short-lived herb, and to discern the mechanisms allowing the plants to reduce the impact of pre-dispersal seed predation. Knowing that the interplay between pre-dispersal seed predators and plants is strongly shaped by the presence of other co-occurring organisms, we tested whether detritivores modulate plant responses towards pre-dispersal seed predators. To do so, we experimentally manipulated in the field pre-dispersal seed predators and detritivores interacting with the short-lived herb Moricandia moricandioides. We found that detritivores did not alter the response of plants to PSPs. Strikingly, the plant overcompensated for pre-dispersal seed predation, almost doubling the number of seeds produced. Plant response to PSPs led to substantial changes in shoot architecture, reproductive traits, chemical defences in leaves and seeds and in seed nutrient content. The overcompensating mechanism seems to be meristem activation, which allowed plants to produce more reproductive tissue, and increasing the proportion of ovules that became seeds, a response which specifically compensates for pre-dispersal seed predation. As far as we know, this is the first experimental evidence of a positive effect of PSPs on plant lifetime fitness as a consequence of plant overcompensation.

Seed size predicts global effects of small mammal seed predation on plant recruitment.

Recent studies demonstrate that by focusing on traits linked to fundamental plant life-history trade-offs, ecologists can begin to predict plant community structure at global scales. Yet, consumers can strongly affect plant communities, and means for linking consumer effects to key plant traits and community assembly processes are lacking. We conducted a global literature review and meta-analysis to evaluate whether seed size, a trait representing fundamental life-history trade-offs in plant offspring investment, could predict post-dispersal seed predator effects on seed removal and plant recruitment. Seed size predicted small mammal seed removal rates and their impacts on plant recruitment consistent with optimal foraging theory, with intermediate seed sizes most strongly impacted globally - for both native and exotic plants. However, differences in seed size distributions among ecosystems conditioned seed predation patterns, with relatively large-seeded species most strongly affected in grasslands (smallest seeds), and relatively small-seeded species most strongly affected in tropical forests (largest seeds). Such size-dependent seed predation has profound implications for coexistence among plants because it may enhance or weaken opposing life-history trade-offs in an ecosystem-specific manner. Our results suggest that seed size may serve as a key life-history trait that can integrate consumer effects to improve understandings of plant coexistence.

Local pesticide use intensity conditions landscape effects on biological pest control.

Complex landscapes including semi-natural habitats are expected to favour natural enemies thereby enhancing natural pest biocontrol in crops. However, when considering a large number of situations, the response of natural biocontrol to landscape properties is globally inconsistent, a possible explanation being that local agricultural practices counteract landscape effects. In this study, along a crossed gradient of pesticide use intensity and landscape simplification, we analysed the interactive effects of landscape characteristics and local pesticide use intensity on natural biocontrol. During 3 years, using a set of sentinel prey (weed seeds, aphids and Lepidoptera eggs), biocontrol was estimated in 80 commercial fields located in four contrasted regions in France. For all types of prey excepted weed seeds, the predation rate was influenced by interactions between landscape characteristics and local pesticide use intensity. Proportion of meadow and length of interface between woods and crops had a positive effect on biocontrol of aphids where local pesticide use intensity was low but had a negative effect elsewhere. Moreover, the landscape proportion of suitable habitats for crop pests decreased the predation of sentinel prey, irrespectively of the local pesticide use intensity for weed seeds, but only in fields with low pesticide use for Lepidoptera eggs. These results show that high local pesticide use can counteract the positive expected effects of semi-natural habitats, but also that the necessary pesticide use reduction should be associated with semi-natural habitat enhancement to guarantee an effective natural biocontrol.

Seed predation does not explain pine invasion success.

Why some non-native plant species invade, and others fail remains an elusive question. Plant invasion success has been associated with specific species traits. Yet, we have limited knowledge of the mechanisms relating these traits to invasion potential. General patterns of biotic resistance by seed predation may provide a mechanism that helps separate invasive from non-invasive plants. Seed predation is an important barrier against plant establishment for many plant species. It may, therefore, create a selective filter against non-native plant establishment based on plant traits related to seed predation rate. In two cafeteria-style seed predation experiments in a steppe ecosystem in Patagonia (Argentina) we provided seeds of 16 non-native Pinaceae covering a 300-fold variation in seed mass, a 200-fold variation in seed volume and 75-fold variation in seed toughness. Seed removal decreased with seed mass and seed volume. Seed toughness was not a significant predictor while seed volume was the best predictor of predators' preference. However, for species of this family small seed size is the most important predictor of species invasiveness. Our results show that seed predation does not explain Pinaceae invasive success. In our system, species that have smaller seeds (i.e., more invasive) are preferentially consumed by seed predators. Seed mass was not the best predictor of granivory rates, despite being the seed trait on which most studies have been focused. Our ability to predict future invasion and understand invasion success could benefit from other studies that focus on the mechanisms behind invasive traits.

Dispersal limitation induces long-term biomass collapse in overhunted Amazonian forests.

Tropical forests are the global cornerstone of biological diversity, and store 55% of the forest carbon stock globally, yet sustained provisioning of these forest ecosystem services may be threatened by hunting-induced extinctions of plant-animal mutualisms that maintain long-term forest dynamics. Large-bodied Atelinae primates and tapirs in particular offer nonredundant seed-dispersal services for many large-seeded Neotropical tree species, which on average have higher wood density than smaller-seeded and wind-dispersed trees. We used field data and models to project the spatial impact of hunting on large primates by ∼ 1 million rural households throughout the Brazilian Amazon. We then used a unique baseline dataset on 2,345 1-ha tree plots arrayed across the Brazilian Amazon to model changes in aboveground forest biomass under different scenarios of hunting-induced large-bodied frugivore extirpation. We project that defaunation of the most harvest-sensitive species will lead to losses in aboveground biomass of between 2.5-5.8% on average, with some losses as high as 26.5-37.8%. These findings highlight an urgent need to manage the sustainability of game hunting in both protected and unprotected tropical forests, and place full biodiversity integrity, including populations of large frugivorous vertebrates, firmly in the agenda of reducing emissions from deforestation and forest degradation (REDD+) programs.

Frequency-dependent seed predation by rodents on Sonoran Desert winter annual plants.

Numerous mechanisms may allow species to coexist. We tested for frequency-dependent predation, a mechanism predicted by theory and established as a foraging behavior for many types of animals. Our field test included multiple prey species exposed in situ to multiple predator species and individuals to determine whether the prey species experienced predation patterns that were frequency dependent. The prey were seeds of three species of Sonoran Desert winter annual plants while the predator species were a guild of nocturnal seed foraging heteromyid and murid rodents that co-occur naturally in the same community as the desert annuals at Tumamoc Hill near Tucson. Seeds of one species were much preferred over the other two. Nonetheless, we found the net effect of rodent foraging to be positively frequency dependent (the preference for each species is higher when it is common than when it is uncommon) as has been previously hypothesized. This frequency-dependent predation should function as a species coexistence promoting mechanism in concert with the storage effect that has been previously demonstrated for this system.

Predation-mediated ecosystem services and disservices in agricultural landscapes.

Ecological intensification may reduce environmental externalities of agriculture by harnessing biodiversity to benefit regulating ecosystem services. However, to propose management options for the production of such services, there is a need to understand the spatiotemporal dynamics of net effects between ecosystem services and disservices provided by wild organisms across taxonomic groups in relation to habitat and landscape management. We studied the contribution of predatory vertebrates and invertebrates (including both carnivores and seed herbivores) to regulating ecosystem services and disservices in 16 cereal fields in response to a local habitat contrast and a landscape complexity gradient. From May to November 2016, we provided weed (predation reflects an ecosystem service) and crop (predation reflects a disservice) seeds, as well as pest (predation reflects an ecosystem service) and beneficial (predation reflects a disservice) invertebrate prey to predators. Seed predation was dominated by vertebrates, while vertebrates and invertebrates contributed equally to predation of animal prey. Before harvest, predation steadily increased from very low levels in May to high levels in July independent of the resource type. After harvest, ecosystem services declined more rapidly than disservices. The presence of adjacent seminatural grasslands promoted crop seed predation, but reduced pest prey predation. Predation on beneficial prey decreased with increasing proportions of seminatural grassland in the landscape. Predatory vertebrates and invertebrates provide important ecosystem services due to the consumption of pests. However, beneficial invertebrates and crop seeds were often consumed to a similar or even higher extent than harmful invertebrates or weed seeds. Our results therefore raise concerns that management options aimed at enhancing service providers may simultaneously increase levels of disservices. By considering positive and negative effects simultaneously, this study addresses an important knowledge gap and highlights the importance of interactions between local management, landscape composition, and service and disservice provision across taxa and over time. Considering trade-offs between ecosystem services and disservices when evaluating the net effects of biodiversity conservation measures on ecosystem service provision is crucial. Future agri-environment schemes that offer payments for seminatural habitats may need to provide higher compensation for farmers in cases where net effects are likely to be negative.