Granivore abundance shapes mutualism quality in plant-scatterhoarder interactions.

Conditional mutualisms involve costs and benefits that vary with environmental factors, but mechanisms driving these dynamics remain poorly understood. Scatterhoarder-plant interactions are a prime example of this phenomenon, as scatterhoarders can either increase or reduce plant recruitment depending on the balance between seed dispersal and predation. We explored factors that drive the magnitude of net benefits for plants in this interaction using a mathematical model, with parameter values based on European beech (Fagus sylvatica) and yellow-necked mice (Apodemus flavicollis). We measured benefits as the percentage of germinating seeds, and examined how varying rodent survival (reflecting, e.g. changes in predation pressure), the rate of seed loss to other granivores, the abundance of alternative food resources, and changes in masting patterns affect the quality of mutualism. We found that increasing granivore abundance can degrade the quality of plant-scatterhoarder mutualism due to increased cache pilferage. Scatterhoarders are predicted to respond by increasing immediate consumption of gathered seeds, leading to higher costs and reduced benefits for plants. Thus, biotic changes that are detrimental to rodent populations can be beneficial for tree recruitment due to adaptive behavior of rodents. When scatterhoarder populations decline too drastically (< 5 individuals ha-1 ); however, tree recruitment may also suffer.

Host body mass, not sex, affects ectoparasite loads in yellow-necked mouse Apodemus flavicollis.

We investigated the presence and potential causes of sex bias in ectoparasite infestations in the yellow-necked mouse Apodemus flavicollis. We compared the natural tick and flea burdens of male and female mice in a temperate beech forest and assessed whether the observed differences were driven by host sex or body mass. We found that males were more heavily infested by ticks compared to female mice. However, this difference was driven by host body mass, and not sex itself. Host body mass positively correlated with flea loads, but there was no evidence of sex bias in flea abundance. In addition, the abundance of both ticks and fleas infesting yellow-necked mice changed over time, both seasonally (month to month) and annually (year to year). Our results underscore the importance of the sexual size dimorphism and the parasite taxon as the primary factors that influence the occurrence of sex-biased parasitism in small mammals.

From trees to fleas: masting indirectly affects flea abundance on a rodent host.

Mast seeding causes strong fluctuations in populations of forest animals. Thus, this phenomenon can be used as a natural experiment to examine how variation in host abundance affects parasite loads. We investigated fleas infesting yellow-necked mice in beech forest after 2 mast and 2 non-mast years. We tested 2 mutually exclusive scenarios: (1) as predicted by classical models of density-dependent transmission, an increase in host density will cause an increase in ectoparasite abundance (defined as the number of parasites per host), versus (2) an increase in host density will cause a decline in flea abundance ("dilution," which is thought to occur when parasite population growth is slower than that of the host). In addition, we assessed whether masting alters the relationship between host traits (sex and body mass) and flea abundance. We found a hump-shaped relationship between host and flea abundance. Thus, the most basic predictions are too simple to describe ectoparasite dynamics in this system. In addition, masting modified seasonal dynamics of flea abundance, but did not affect the relationship between host traits and flea abundance (individuals with the highest body mass hosted the most fleas; after controlling for body mass, parasite abundance did not vary between sexes). Our results demonstrate that pulses of tree reproduction can indirectly, through changes in host densities, drive patterns of ectoparasite infestation.

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.

Body mass and sex, but not breeding condition and season, influence open-field exploration in the yellow-necked mouse.

Theory predicts that risk taking should be influenced by external (e.g., season) and internal (e.g., breeding condition, sex, and body mass) conditions. We investigated whether these factors are associated with a potentially risky behavior: exploration of a novel environment. We conducted repeated open-field tests of exploration in a common forest rodent, the yellow-necked mouse Apodemus flavicollis. Contrary to expectations, the exploration did not vary with the season (spring vs. fall) or the reproductive status of the tested animals. Also unexpectedly, there was an inverted U-shaped relationship between body mass and exploration: animals with intermediate body mass tended to have the highest exploration tendencies. Males were more exploratory than females. Finally, even after adjusting for the effects of body mass and sex, individuals exhibited consistent, repeatable differences in exploration tendencies ("behavioral types" or "personalities"). The discrepancies between certain broad generalizations and our results suggest that risk taking depends on details of species-specific biology.

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.

Mast seeding promotes evolution of scatter-hoarding.

Many plant species worldwide are dispersed by scatter-hoarding granivores: animals that hide seeds in numerous, small caches for future consumption. Yet, the evolution of scatter-hoarding is difficult to explain because undefended caches are at high risk of pilferage. Previous models have attempted to solve this problem by giving cache owners large advantages in cache recovery, by kin selection, or by introducing reciprocal pilferage of 'shared' seed resources. However, the role of environmental variability has been so far overlooked in this context. One important form of such variability is masting, which is displayed by many plant species dispersed by scatterhoarders. We use a mathematical model to investigate the influence of masting on the evolution of scatter-hoarding. The model accounts for periodically varying annual seed fall, caching and pilfering behaviour, and the demography of scatterhoarders. The parameter values are based mostly on research on European beech (Fagus sylvatica) and yellow-necked mice (Apodemus flavicollis). Starvation of scatterhoarders between mast years decreases the population density that enters masting events, which leads to reduced seed pilferage. Satiation of scatterhoarders during mast events lowers the reproductive cost of caching (i.e. the cost of caching for the future rather than using seeds for current reproduction). These reductions promote the evolution of scatter-hoarding behaviour especially when interannual variation in seed fall and the period between masting events are large. This article is part of the theme issue 'The ecology and evolution of synchronized seed production in plants'.

Intrinsic and extrinsic drivers of intraspecific variation in seed dispersal are diverse and pervasive.

There is growing realization that intraspecific variation in seed dispersal can have important ecological and evolutionary consequences. However, we do not have a good understanding of the drivers or causes of intraspecific variation in dispersal, how strong an effect these drivers have, and how widespread they are across dispersal modes. As a first step to developing a better understanding, we present a broad, but not exhaustive, review of what is known about the drivers of intraspecific variation in seed dispersal, and what remains uncertain. We start by decomposing 'drivers of intraspecific variation in seed dispersal' into intrinsic drivers (i.e. variation in traits of individual plants) and extrinsic drivers (i.e. variation in ecological context). For intrinsic traits, we further decompose intraspecific variation into variation among individuals and variation of trait values within individuals. We then review our understanding of the major intrinsic and extrinsic drivers of intraspecific variation in seed dispersal, with an emphasis on variation among individuals. Crop size is the best-supported and best-understood intrinsic driver of variation across dispersal modes; overall, more seeds are dispersed as more seeds are produced, even in cases where per seed dispersal rates decline. Fruit/seed size is the second most widely studied intrinsic driver, and is also relevant to a broad range of seed dispersal modes. Remaining intrinsic drivers are poorly understood, and range from effects that are probably widespread, such as plant height, to drivers that are most likely sporadic, such as fruit or seed colour polymorphism. Primary extrinsic drivers of variation in seed dispersal include local environmental conditions and habitat structure. Finally, we present a selection of outstanding questions as a starting point to advance our understanding of individual variation in seed dispersal.

Complex and Diverse Drivers of Parasite Loads in a Cosmopolitan Insect.

The goal of parasite epidemiologists is to understand the factors that determine host infection levels. Potential infection determinants exist at many scales, including spatial and temporal environmental variation, among-host differences, and interactions between symbionts infecting the same host. All of these factors can impact levels of parasitism, but frequently only a subset is considered in any host-parasite system. We examined several potential determinants of pinworm infection in wild Australian cockroaches (Periplaneta australasiae) from multiple biological scales: (1) habitat; (2) season; (3) cockroach body size, developmental stage, and sex; and (4) interactions between 2 pinworm species (Leidynema appendiculata and Thelastoma sp.). Over 1 yr, we collected 239 cockroaches from 2 separate rooms in an Illinois greenhouse. We used generalized linear mixed-effects models (GLMMs) to evaluate simultaneously the influence of these factors on pinworm abundance, and nearly all had significant effects. Overall, the abundance of L. appendiculata was greater than Thelastoma sp., but the relative abundance of the 2 species was reversed in each room (i.e., a taxon × habitat effect). Abundance varied over 4 trapping seasons and increased with cockroach size. Adult cockroaches had more pinworms than nymphs, and there was also a significant taxon × stage effect: adult cockroaches had fewer pinworms than expected for their larger size, and this reduction was greater in Thelastoma sp. than in L. appendiculata. Cockroach sex had no effect on infection. Although females had more worms than males, this difference could be explained by the larger size of females. Finally, after controlling for all other potential determinants of infection, we found a strong negative association between Thelastoma sp. and L. appendiculata; cockroaches tended to be infected with either 1 pinworm species or the other. Our work underscores the importance of measuring potential determinants of infection from as many scales as possible. Such approaches are necessary to unravel the complexities of host-parasite interactions.

Consequences of intraspecific variation in seed dispersal for plant demography, communities, evolution and global change.

As the single opportunity for plants to move, seed dispersal has an important impact on plant fitness, species distributions and patterns of biodiversity. However, models that predict dynamics such as risk of extinction, range shifts and biodiversity loss tend to rely on the mean value of parameters and rarely incorporate realistic dispersal mechanisms. By focusing on the mean population value, variation among individuals or variability caused by complex spatial and temporal dynamics is ignored. This calls for increased efforts to understand individual variation in dispersal and integrate it more explicitly into population and community models involving dispersal. However, the sources, magnitude and outcomes of intraspecific variation in dispersal are poorly characterized, limiting our understanding of the role of dispersal in mediating the dynamics of communities and their response to global change. In this manuscript, we synthesize recent research that examines the sources of individual variation in dispersal and emphasize its implications for plant fitness, populations and communities. We argue that this intraspecific variation in seed dispersal does not simply add noise to systems, but, in fact, alters dispersal processes and patterns with consequences for demography, communities, evolution and response to anthropogenic changes. We conclude with recommendations for moving this field of research forward.

Rapid aggregative and reproductive responses of weevils to masting of North American oaks counteract predator satiation.

The predator satiation hypothesis posits that masting helps plants escape seed predation through starvation of predators in lean years, followed by satiation of predators in mast years. Importantly, successful satiation requires sufficiently delayed bottom-up effects of seed availability on seed consumers. However, some seed consumers may be capable of quick aggregative and reproductive responses to masting, which may jeopardize positive density dependence of seed survival. We used a 17-yr data set on seed production and insect (Curculio weevils) infestation of three North American oaks species (northern red Quercus rubra, white Q. alba, and chestnut oak Q. montana) to test predictions of the predation satiation hypothesis. Furthermore, we tested for the unlagged numerical response of Curculio to acorn production. We found that masting results in a bottom-up effect on the insect population; both through increased reproductive output and aggregation at seed-rich trees. Consequently, mast seeding in two out of three studied oaks (white and chestnut oak) did not help to escape insect seed predation, whereas, in the red oak, the escape depended on the synchronization of mast crops within the population. Bottom-up effects of masting on seed consumer populations are assumed to be delayed, and therefore to have negligible effects on seed survival in mast years. Our research suggests that insect populations may be able to mount rapid reproductive and aggregative responses when seed availability increases, possibly hindering satiation effects of masting. Many insect species are able to quickly benefit from pulsed resources, making mechanisms described here potentially relevant in many other systems.

Invasive oaks escape pre-dispersal insect seed predation and trap enemies in their seeds.

Species introduced to habitats outside their native range often escape control by their natural enemies. Besides competing with native species, an alien species might also affect the native herbivores by introducing a new source of different quality food. Here, we describe the case of northern red oak (Quercus rubra) invasion in Europe. We collected data on insect (moth Cydia spp. and weevil Curculio spp.) seed predation of northern red oak in its native (USA, North America) and invasive (Poland, Europe) range, as well as for sessile oaks (Quercus petrea) in Europe. We also evaluated the quality of acorns as hosts for weevil larvae by collecting infested acorns and measuring weevil developmental success, and quantifying acorn traits such as seed mass, tannins, lipids and protein concentration. We used DNA barcoding to identify insects to the species level. The predation by moths was similar and very low in both species and in both ranges. However, red oaks escape pre-dispersal seed predation by weevils in Europe. Weevil infestation rates of northern red oak acorns in their invasive range were 10 times lower than that of sessile oaks, and also 10 times lower than that of red oaks in North America. Furthermore, even when weevils oviposited into northern red oaks, the larvae failed to develop, suggesting that the exotic host created a trap for the insect. This phenomenon might gradually decrease the local abundance of the seed predator, and further aid the invasion.

How intraspecific variation in seed-dispersing animals matters for plants.

Seed dispersal by animals is a complex phenomenon, characterized by multiple mechanisms and variable outcomes. Most researchers approach this complexity by analysing context-dependency in seed dispersal and investigating extrinsic factors that might influence interactions between plants and seed dispersers. Intrinsic traits of seed dispersers provide an alternative way of making sense of the enormous variation in seed fates. I review causes of intraspecific variability in frugivorous and granivorous animals, discuss their effects on seed dispersal, and outline likely consequences for plant populations and communities. Sources of individual variation in seed-dispersing animals include sexual dimorphism, changes associated with growth and ageing, individual specialization, and animal personalities. Sexual dimorphism of seed-dispersing animals influences seed fate through diverse mechanisms that range from effects caused by sex-specific differences in body size, to influences of male versus female cognitive functions. These differences affect the type of seed treatment (e.g. dispersal versus predation), the number of dispersed seeds, distance of seed dispersal, and likelihood that seeds are left in favourable sites for seeds or seedlings. The best-documented consequences of individual differences associated with growth and ageing involve quantity of dispersed seeds and the quality of seed treatment in the mouth and gut. Individual specialization on different resources affects the number of dispersed plant species, and therefore the connectivity and architecture of seed-dispersal networks. Animal personalities might play an important role in shaping interactions between plants and dispersers of their seeds, yet their potential in this regard remains overlooked. In general, intraspecific variation in seed-dispersing animals often influences plants through effects of these individual differences on the movement ecology of the dispersers. Two conditions are necessary for individual variation to exert a strong influence on seed dispersal. First, the individual differences in traits should translate into differences in crucial characteristics of seed dispersal. Second, individual variation is more likely to be important when the proportions of particular types of individuals fluctuate strongly in a population or vary across space; when proportions are static, it is less likely that intraspecific differences will be responsible for changes in the dynamics and outcomes of plant-animal interactions. In conclusion, focusing on variation among foraging animals rather than on species averages might bring new, mechanistic insights to the phenomenon of seed dispersal. While this shift in perspective is unlikely to replace the traditional approach (based on the assumption that all important variation occurs among species), it provides a complementary alternative to decipher the enormous variation observed in animal-mediated seed dispersal.

Deciphering the effects of disperser assemblages and seed mass on patterns of seed dispersal in a rodent community.

The sizes of both seed dispersers and seeds are traits that are likely to interact to influence seed fate in many synzoochoric plant species. Here, we examined whether members of a granivorous rodent community consisting of species of different body size vary in their effectiveness as seed dispersers, and how this relationship may be altered by seed size. We marked northern red oak (Quercus rubra) acorns with plastic tags and placed them in size-selective rodent exclosures. The exclosures allowed differential access of rodent groups based on different body size: (i) small (e.g. Peromyscus spp.); (ii) small and medium (e.g. Tamias striatus); and (iii) small, medium and large (e.g. Sciurus carolinensis) species of rodents. Acorn removal did not differ among exclosure types, but more seeds were missing when removed by small rodents, probably because of larderhoarding. The treatments did not influence the relative frequency of acorn consumption. However, small rodents cached considerably fewer and partially ate more acorns than the other 2 groups. The mean dispersal distance was the longest for cages with medium openings, intermediate for cages with large openings and the shortest for cages with small openings. Acorn mass positively affected the probability of caching and this relationship was unaffected by exclosure type. In conclusion, granivorous rodents of different body sizes strongly differed in their interactions with acorns, with small rodents acting primarily as acorn predators and medium and large species contributing significantly more to dispersal of red oaks.

Negative effects of density on space use of small mammals differ with the phase of the masting-induced population cycle.

Home range size generally decreases with increasing population density, but testing how this relationship is influenced by other factors (e.g., food availability, kin structure) is a difficult task. We used spatially explicit capture-recapture models to examine how home range size varies with population density in the yellow-necked mouse (Apodemus flavicollis). The relationship between population density and home range size was studied at two distinct phases of population fluctuations induced by beech (Fagus sylvatica) masting: post-mast peak in abundance (first summer after mast, n = 2) and subsequent crash (second summer after mast, n = 2). We live-trapped mice from June to September to avoid the confounding effects of autumn seedfall on home range size. In accordance with general predictions, we found that home range size was negatively associated with population density. However, after controlling for the effect of density, home ranges of mice were larger in post-mast years than during the crash phase. This indicates a higher spatial overlap among neighbors in post-mast years. We suggest that the increased spatial overlap is caused by negative density-dependent dispersal that leads to high relatedness of individuals within population in the peak phase of the cycle.

Advantages of masting in European beech: timing of granivore satiation and benefits of seed caching support the predator dispersal hypothesis.

The predator satiation and predator dispersal hypotheses provide alternative explanations for masting. Both assume satiation of seed-eating vertebrates. They differ in whether satiation occurs before or after seed removal and caching by granivores (predator satiation and predator dispersal, respectively). This difference is largely unrecognized, but it is demographically important because cached seeds are dispersed and often have a microsite advantage over nondispersed seeds. We conducted rodent exclosure experiments in two mast and two nonmast years to test predictions of the predator dispersal hypothesis in our study system of yellow-necked mice (Apodemus flavicollis) and European beech (Fagus sylvatica). Specifically, we tested whether the fraction of seeds removed from the forest floor is similar during mast and nonmast years (i.e., lack of satiation before seed caching), whether masting decreases the removal of cached seeds (i.e., satiation after seed storage), and whether seed caching increases the probability of seedling emergence. We found that masting did not result in satiation at the seed removal stage. However, masting decreased the removal of cached seeds, and seed caching dramatically increased the probability of seedling emergence relative to noncached seeds. European beech thus benefits from masting through the satiation of scatterhoarders that occurs only after seeds are removed and cached. Although these findings do not exclude other evolutionary advantages of beech masting, they indicate that fitness benefits of masting extend beyond the most commonly considered advantages of predator satiation and increased pollination efficiency.

Ectoparasite loads in sympatric urban populations of the northern white-breasted and the European hedgehog.

We investigated abundance and prevalence of ticks and fleas infesting urban populations of two species of hedgehogs: the northern white-breasted hedgehog (Erinaceus roumanicus) and the European hedgehog (Erinaceus europaeus). The hedgehogs were captured in the city of Poznan (western Poland) over the period of 4 years. Both species of hedgehogs were infested with the castor bean tick (Ixodes ricinus), the hedgehog tick (Ixodes hexagonus), and the hedgehog flea (Archeopsylla erinacei). The northern white-breasted hedgehog had higher loads of I. ricinus and A. erinacei than the European hedgehog. The abundance and prevalence of I. hexagonus were similar on both species of hosts. Co-infestation with the two species of ticks was more frequent on the northern white-breasted hedgehog than on the European hedgehog. Therefore, these two closely related species of hedgehogs differ in their importance as hosts of arthropod vectors of pathogens in urban areas and might play a different role in the dynamics of zoonotic diseases.

Fire and mice: seed predation moderates fire's influence on conifer recruitment.

In fire-adapted ecosystems, fire is presumed to be the dominant ecological force, and little is known about how consumer interactions influence forest regeneration. Here, we investigated seed predation by deer mice (Peromyscus maniculatus) and its effects on recruitment of ponderosa pine (Pinus ponderosa) and Douglas-fir (Pseudotsuga menziesii) seedlings in unburned and recently burned fire-adapted montane forests in west-central Montana, USA. Deer mice were almost twice as abundant in burned than unburned stands. Deer mouse removal of seeds from petri dishes was two times higher in burned than in unburned stands, and seed removal levels were 8% higher for ponderosa pine than for the smaller Douglas-fir seeds. In seed-addition experiments, emergence of seedlings in deer mouse-exclusion cages was almost six times higher in burned compared to unburned forest. In both burned and unburned forest, emergence was lower for ponderosa pine than for Douglas-fir. Seedling survival to establishment did not differ between conifer species but was considerably higher in burned than in unburned forest. However, effects of seed predation on recruitment prevailed over fire effects: in cages allowing access by deer mice, emergence and establishment were extremely rare for both conifer species in both burned and unburned forest. This research suggests that consumer interactions can substantially influence recruitment even in fire-adapted forest ecosystems.