Rafał Zwolak

Responses of small mammals to clear-cutting in temperate and boreal forests of Europe: a meta-analysis and review

Abstract We analyzed the responses of small mammals to clear-cutting in temperate and boreal forests in Europe. We conducted a meta-analysis of published research on most often studied small mammal species (the striped field mouse, the yellow-necked mouse, the wood mouse, the field vole, the common vole, the bank vole, the Eurasian harvest mouse, the common shrew and the Eurasian pygmy shrew), comparing their abundance on clear-cuts and in unharvested stands. For four other species (the gray-sided vole, the Siberian flying squirrel, the Eurasian red squirrel and the hazel dormouse), we provide a qualitative review of their responses to forest harvest. Results of the meta-analysis suggest that common species of small mammals usually increase in abundance after clear-cutting or are unaffected by this disturbance. As an exception, the yellow-necked mouse declines after clear-cutting in boreal but not in temperate forest. The qualitative review suggests that the responses of more specialized (e.g., arboreal) species to forest harvest are more varied than the responses of generalist species included in the meta-analysis. For some species of small mammals (e.g., the Siberian flying squirrel), habitat loss resulting from forest harvest is a major threat.

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.

Effects of nitrogen deposition on reproduction in a masting tree: benefits of higher seed production are trumped by negative biotic interactions

Summary Relatively little is known about the effects of anthropogenic environmental changes on reproductive ecology of trees. Yet, recruitment is a primary determinant of the long-term dynamics of plant populations in changing environments. We used the Long-Term Ecological Research site at Harvard Forest to evaluate the effects of chronic (over 25 years) nitrogen fertilization on reproductive ecology of red oaks (Quercus rubra). Oaks growing in fertilized plots produced 4-9 times more acorns than control trees. However, nitrogen deposition simultaneously affected oaks’ biotic interactions. It increased pre-dispersal seed predation by insects (primarily weevils, Curculio spp.) on fertilized plots, most likely as the result of the disruption of predator satiation. In addition, infestation by weevils was more likely to result in embryo destruction in fertilized than in control acorns. Furthermore, the proportion of acorns dispersed and cached by rodents decreased on fertilized plots. Finally, germination of fertilized acorns was lower than control acorns, even after controlling for effects of weevils and rodents. Inclusion of the altered biotic interactions reversed the final picture of the effects of long-term nitrogen fertilization on oak reproduction: the positive effects on acorn quantity were trumped by the nitrogen-mediated changes in biotic interactions. Synthesis. Our results stress the importance of considering indirect effects and consumer interactions when evaluating effects of environmental change on plant population dynamics. Long-term nitrogen fertilization has a strong potential to decrease the recruitment of masting trees. Given the ubiquitous increase in the anthropogenic nitrogen deposition, processes similar to those found in our system might operate in others, resulting in a widespread alteration of trees’ recruitment dynamics. This article is protected by copyright. All rights reserved.

Behavioural mechanisms of conflict avoidance among shrews

Stable co-existence of similar species should be facilitated by mechanisms impairing, besides exploitative, interference competition. We investigated avoidance of intra- and interspecific conflicts in a four-species community of shrews [Sorex minutus Linnaeus, 1766,S. araneus Linnaeus, 1758,Neomys anomalus Cabrera, 1907, andN. fodiens (Pennant, 1771)], using the method of dyadic encounters in a neutral arena. We tested whether the use of passive (habituation, reduction of mobility, increase of inter-individual distance, and stillness) and active (‘to-and-fro’ and ‘keeping distance’ behaviours) forms of conflict avoidance depends on species, size or domination rank. The duration of conflicts was positively correlated with mobility and negatively with inter-individual distance, whereas it was unrelated to time of stillness and the active forms. The repertoire of conflict avoidance mechanisms was not species-specific and the display of these mechanisms depended rather on the size and domination rank of animals participating in a given interaction. In contrast to rodents, shrews did not avoid conflicts by the most passive forms: freeze and stillness reactions. All other forms were used with a higher or lower efficiency by all species. However, consistent with our predictions, large shrews (asN. fodiens) used mainly the passive mechanisms of conflicts avoidance (‘wait-and-see’ strategy), whereas small shrews (asS. minutus) invest proportionally more time in active forms (‘escape’ strategy).

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.

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.

Reduced ectoparasite loads of deer mice in burned forest: From fleas to trees?

We tested whether reduced parasite loads might contribute to high post-fire abundances of deer mice (Peromyscus maniculatus). We performed parasite examinations of 54 mice captured in burned forest in the area of Davis Fire (western Montana, USA), and 26 mice captured in nearby unburned forest. Mean abundance of ectoparasites (fleas, ticks, and lice) was lower in burned than in unburned forest. The difference was particularly pronounced for fleas, which were reduced by 70% in burned forest. Endoparasites (i.e., nematodes and cestodes) were unaffected. Mechanisms for the lower mean abundance of fleas in burned areas are not known, but might involve flea mortality in burrows during fire or decreased transmission, survival, or both in the post-fire environment. We propose several hypothetical pathways through which reduced ectoparasite loads could cause an increase in deer mouse abundance, such as improved health status or increased foraging efficiency of mice, both of which could translate into the increased reproduction that has been reported in mice from burned forest. We encourage experimental tests of the ectoparasite release hypothesis of the post-fire increase in deer mouse abundance.

Simultaneous population fluctuations of rodents in montane forests and alpine meadows suggest indirect effects of tree masting

Resource pulses can generate cross-habitat dispersal of consumers, and therefore affect organisms even in areas where the resource pulses do not occur. We investigated this phenomenon at the elevational treeline in the Carpathian Mountains, where beech (Fagus sylvatica) masting caused an increase in abundance of forest rodents and intensified their use of alpine meadows. We tested 3 hypotheses concerning the impact of forest rodent spillover on the abundance of meadow-dwelling pine voles (Microtus subterraneus): 1) the competition hypothesis: if the spillover affects pine voles mostly through intensified competitive interactions, then pine voles should decline when forest rodents reach their peak abundance, i.e., 1 year after masting; 2) the apparent competition hypothesis: if predators switch to alternative prey when populations of forest rodents collapse, then pine voles should decline 2 years after masting; and 3) the apparent mutualism hypothesis: if the increase of forest rodents temporarily releases pine voles from predatory pressure, pine voles should increase in synchrony with forest rodents—1 year after masting. Our results, while correlative in nature, supported the apparent mutualism hypothesis: 1 year after masting, both forest rodents and pine voles strongly increased their abundance. Two years after masting, when populations of forest rodents crashed, abundance of pine voles returned to pre-masting levels rather than collapse. These findings suggest that pulsed spillover, known mostly from negative effects on organisms in recipient habitats, can also create indirect positive interactions. Furthermore, they illustrate how density-dependent spillover of animals might increase the spatial scale of masting effects beyond the habitats where seeds are released.

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

Abstract 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.

Predators or mutualists? Lack of dispersal distance benefits and small caching profits makes scatterhoarding rodents antagonists of oaks

Numerous interactions between plants and animals vary in their outcome between antagonism and mutualism, but it proved to be difficult to quantify their final outcome. Interactions between plants and scatterhoarding animals provide a prime example of this phenomenon. Scatterhoarders consume large quantities of seeds (potentially reducing plant establishment), yet also disperse seeds and bury them in shallow caches (potentially improving recruitment). However, it has been rarely determined which role prevails for particular plant species. We experimentally evaluated the benefits of rodent seed dispersal in two model oak species (sessile oak Quercus petraea, and red oak Q. rubra) and used a heuristic mathematical model to place the interactions at the antagonism-mutualism continuum. Our results indicate that during the period of the study, interactions between scatterhoarding rodents and both focal oaks were antagonistic. Even though acorn burial increased the likelihood of seedling establishment, this effect was not strong enough to compensate for the costs of seed predation. Furthermore, we found no evidence that the short-distance transportation that is usually provided by small mammals benefits early oak recruitment. Even relatively large improvements in seedling establishment after seed burial do not necessarily render the plant-scatterhoarder interaction mutualistic. Our study is the first to separate and directly quantify two most important services provided to plants by their rodent partners: seed transportation away from parent plants and seed burial in topsoil. It also demonstrates how readily accessible field data can be used to gauge the outcomes in plant-granivore conditional mutualisms.Numerous interactions between plants and animals vary in their outcome between antagonism and mutualism, but it has proven to be difficult to quantify their final outcome. Interactions between plants and scatterhoarding animals provide a prime example of this phenomenon. Scatterhoarders consume large quantities of seeds (potentially reducing plant establishment), yet also disperse seeds and bury them in shallow caches (potentially improving recruitment). However, it has been rarely determined which role prevails for particular plant species. We demonstrate how plant-scatterhoarder interactions can be placed at the antagonism-mutualism continuum, with interactions between rodents and two oaks species (sessile oak Quercus petraea, and red oak Q. rubra) as an empirical example. Our approach consists of quantifying the net outcome of the interaction through assembling different vital rates (e.g. probability of seedling recruitment with and without rodents; near and far from conspecific trees; with and without seed pilferage) piecewise with a simple mathematical model. Our results indicate that during the period of the study, interactions between scatterhoarding rodents and both focal oaks were antagonistic. Even though acorn burial increased the likelihood of seedling establishment, this effect was not strong enough to compensate for the costs of seed predation. Furthermore, we found no evidence that the short-distance transportation that is usually provided by small mammals benefited early oak recruitment. Our study demonstrates how readily accessible field data can be used to gauge the outcomes in conditional mutualisms.