Rodents are well known as both seed predators and dispersers of various plant species in forest ecosystems, and they play an important role in the regeneration of vegetation. Thus, the research on seed selection and vegetation regeneration by sympatric rodents is an interesting topic. To understand the characteristics of preferences of rodents for different seeds, a semi-natural enclosure experiment was performed with four rodent species (Apodemus peninsulae, Apodemus agrarius, Tscherskia triton, and Clethrionomys rufocanus) and the seeds of seven plant species (Pinus koraiensis, Corylus mandshurica, Quercus mongolica, Juglans mandshurica, Armeniaca sibirica, Prunus salicina, and Cerasus tomentosa) to investigate the differentiation in niches and patterns of resource utilization of sympatric rodents. The results showed that all the rodents had consumed many seeds of Pi. koraiensis, Co. mandshurica, and Q. mongolica but differed significantly in how they selected the different seeds. The rate of utilization (R_i) of Pi. koraiensis, Co. mandshurica, and Q. mongolica exhibited the highest values. The E_i values indicated that the rodents tested exhibited differences in their priorities used to select the seeds from different plant species. All four species of rodents exhibited obvious preferences for certain seeds. Korean field mice preferentially consumed the seeds of Q. mongolica, Co. mandshurica, and Pi. koraiensis. Striped field mice favor the seeds of Co. mandshurica, Q. mongolica, P. koraiensis, and Nanking cherry. Greater long-tailed hamsters prefer to consume the seeds of Pi. koraiensis, Co. mandshurica, Q. mongolica, Pr. salicina, and Ce. tomentosa. Clethrionomys rufocanus likes to eat the seeds of Pi. koraiensis, Q. mongolica, Co. mandshurica, and Ce. tomentosa. The results supported our hypothesis that sympatric rodents overlap in food selection. However, each rodent species has a marked preference for food selection, and different rodent species differ in their food preferences. This reflects the role of distinct food niche differentiation in their coexistence.

Coexistence, competition, fitness, food selection, niche, niche differentiation

The coexistence of species and the maintenance of biodiversity are important topics of ecological study. Food is an essential resource for survival, so there are obvious effects of differences in food selection and feeding behavior among animal species on their coexistence. Furthermore, the food choices of animals directly affect their survival and reproduction. However, the factors that affect the selection of food by animals in forest ecosystems are very complicated, and the choices of different rodent species of the seeds from different plant species depend on many factors. The characteristics of the seeds of different plant species vary by size (Vander Wall 2001; Xiao et al. 2005; Chang and Zhang 2014; Luna et al. 2016); the contents of nutrients, tannins, and other secondary metabolites (Steele et al. 1993; Wang and Chen 2012; Chang and Zhang 2014); and the hardness and thickness of the seed coat (Li et al. 2018). All these factors affect the food choices of rodent species and further influence their behavior (Li et al. 2018).

The selective foraging of all animals is a key factor that affects their survival and reproduction. Animals in nature generally exhibit food preference or selective foraging (Hughes and Croy 1993), and no animal uses all the food types that occur in the environment equally, particularly when there are other competing species. In general, animals only prefer a small fraction of the available foods. They rarely feed on most foods and even completely reject some. Effective food preference ensures that animals efficiently intake energy and nutrients and maximize their food selection fitness (Moss 1991; Rogers and Blundell 1991).

Large seeds produced by many plant species are a valuable food source for rodents, which often prefer certain seeds from various plant species within their habitats and are capable of accurately distinguishing the seeds with different characteristics (Vander Wall 2001; Chang and Zhang 2014; Luna et al. 2016; Li et al. 2018). Their identification and choice of food affects the fate of seeds, while the rodents must weigh the input costs (time and energy) when foraging to utilize different eating and dispersal strategies to ensure supplies of optimal food and energy (Vander Wall 1990; Lima 1998; Li et al. 2021).

Seed characteristics, including size and weight (Vander Wall 2001; Luna et al. 2016); seed coat characteristics, such as thickness and hardness (Vander Wall 1990; Luna et al. 2016; Li et al. 2018); seed quality, such as seeds damaged by pests, mildewed, or empty-shelled (Vander Wall 1990; Chang et al. 2010; Vander Wall 2010; Wang et al. 2012); moisture content; nutrients, such as starch, fat, and protein (Vander Wall 1990; Vander Wall 2001); and secondary metabolic compounds, such as tannins and other polyphenolics (Steele et al. 1993; Wang and Chen 2012; Chang and Zhang 2014) affect the decision making of rodents during food selection. Most studies have shown that seed size and nutrients are key factors that determine the foraging strategies of animals, and rodents usually prefer large seeds that are rich in nutrients (Smith and Reichman 1984; Xiao et al. 2006). Harper et al. (1970) strongly suggested that large seeds are favored because they provide a greater return to the seed predators. The optimal foraging theory (OFT; Charnov 1976) suggests that animals favor seeds that generate the largest net return. In general, the total return in foraging increases as the seed size increases, and during the same duration of foraging, the probability that large seeds with higher nutritional content and benefit will be eaten is higher because such foods can better compensate the energy expenditure by the animal during foraging and thus, are more attractive (Xiao et al. 2005; Luna et al. 2016).

The time that seeds are handled is another important factor that influences animal behavior and decision making, and it significantly affects the foraging strategy of rodents (Jacobs 1992; Chang et al. 2010; Li et al. 2020). Because the time of seed handling is associated with the weighing of predation risk against foraging efficiency (Chang et al. 2010; Wang et al. 2012; Li et al. 2020), it tends to be minimized by rodents to enhance survival. The choice of food by rodents is also affected by the size and ability of the individual. A rodent will set an upper threshold for the preferred seed size based on its own size, so seeds from the same plant species may provide very different net returns to varying predators (Jacobs 1992; Luna et al. 2016). Because of differences in body size, strength and mouth type, predators differ in their ability to handle different seeds.

Studies of animal food choice are significant to understand the co-evolution of animal and plant systems, as well as niche differentiation among sympatric animals (Vander Wall 2001; Li and Zhang 2003; Vander Wall and Beck 2011; Li et al. 2018). Since rodents are the primary predators and dispersers of seeds in forest ecosystems (Vander Wall 1990), they form a system of foraging and reciprocity with seeds. The degree of preference of rodents for a certain type of seed and the differential selection of different seeds can lead to changes in predation pressure and the rate of dispersion among plant species (Pons and Pausas 2006), and it may have important impacts on seed dispersal and the natural regeneration of forest communities through the heavy consumption of seeds by animals (Vander Wall 1990; Perea et al. 2011; Li et al. 2021). Their consumption can distribute seeds and lead to seedling establishment as a result of hoarding behavior (Janzen 1971; Grubb 1977; Clark and Clark 1984; Willson and Whelan 1990; Vander Wall 2001; Briggs et al. 2009). The seed mortality owing to the foraging of animals affects the fitness, population structure, and composition of species of the plant community (Willson and Whelan 1990). The competition for resources among sympatric animals has been an important topic in community ecology, and numerous studies have shown that competition is the primary factor that causes variation in the use of resources by animals, thus, leading to differences in morphology and behavioral strategies among species.

Currently, the differential selection of seeds of a given plant species by sympatric rodent species has not been well researched. In this study, we used four sympatric rodent species and the seeds of seven plant species distributed in northern temperate forests to investigate the differences in seed choice related to the species under semi-natural enclosure conditions, as well as the effect of seed characteristics on the strategic differentiation in food choice by rodents to gain insight into the niche partitioning of sympatric rodents and its effect on the fate of the seeds of specific plants and vegetation renewal. We hypothesized that sympatric rodents feed on largely similar food items but differ significantly in their preferred choices.

Analyses of food consumption, the order of seed selection, and E_i demonstrated that the four rodent species in this study all favored or preferred the seeds of Pi. koraiensis, Co. mandshurica, and Q. mongolica. These seeds are large and commonly found in boreal forests that have high numbers of J. mandshurica of the appropriate sizes, easily handled, and containing abundant resources. Thus, they have become a favored food for most species of small rodents during the long natural process of evolution. Furthermore, the long history of competition has led to food niche differentiation in sympatric rodents, whose preference for the seeds of certain plant species has largely been demonstrated in this work. Among the three plant species most favored, A. peninsulae preferred the seeds of Q. mongolica; A. agrarius preferred the seeds of Co. mandshurica, and Cl. rufocanus preferred the seeds of Pi. koraiensis. Tscherskia triton exhibited no preference. The preferences of the four rodent species for the seeds of different plant species reflect a mutually beneficial symbiotic relationship that has evolved over a long time. As food resources, the seeds of these plants provide the necessary nutrients for the survival and reproduction of these rodents and thus, affect animal behavior and population dynamics (Janzen 1971; Vander Wall 2001; Luna et al. 2016; Li et al. 2018). The foraging, transportation, and hoarding of plant seeds and fruits by these rodent species influences the spread and renewal of vegetation (Janzen 1971; Grubb 1977; Clark and Clark 1984; Willson and Whelan 1990; Vander Wall 2001; Briggs et al. 2009; Li et al. 2021).

Intrinsic factors of a rodent, such as its body size and ability to process food, also exert important effects on its food selection. Among the four rodent species tested in this study, T. triton is the largest in body size followed by A. peninsulae, while A. agrarius and Cl. rufocanus are smaller. The large-sized T. triton therefore has a higher capacity for handling food and consumed all the seeds of Pi. koraiensis, Co. mandshurica, and Q. mongolica, as well as most of the seeds of A. sibirica, Pr. salicina, and Ce. tomentosa. Furthermore, its E_i values demonstrated that it favors seeds from additional plant species, indicating that the diet breadth and eating capacity of T. triton are higher than those of each of the other three rodent species. The food preference of T. triton was not as refined as that of other species, possibly because the supply of its favored seed resources is too small to meet its large demand for food, so it must exploit other seed resources.

According to the Optimal Foraging Theory, natural selection has enabled animals to maximize their net benefits during foraging, and the most efficient foraging strategy ensures survival and reproductive success (Charnov 1976). Many small rodent species have been found to not feed on the seeds of J. mandshurica, and A. peninsulae only consumed a small percentage (23.08%) of these seeds. This resulted in an R_i that only accounted for 4.08% of its total food consumption. This result is related to the seed-handling ability of the rodents. Although the seeds of J. mandshurica are rich in nutrients and can provide more benefit in a single seed, they are large and have a hard seed coat, which pose substantial challenges to small rodents during both transport and consumption, making it difficult for them to substantially benefit from the seeds (Xiao et al. 2005). This is consistent with the result of our field studies (unpublished results) that showed the small rodents rarely chose the seeds of J. mandshurica. The preferences of the four rodent species in this study for the seeds of A. sibirica, Pr. salicina, and Ce. tomentosa, three sparsely distributed plant species, varied markedly, and the consumption of Ce. tomentosa seeds by A. agrarius and Cl. rufocanus was greater than that of A. sibirica or Pr. salicina, likely owing to differences in the seed-handling abilities of the different species. Apodemus agrarius and Cl. rufocanus are the smallest rodents and therefore, must invest tremendous effort to handle the seeds of A. sibirica and Pr. salicina with their thick, hard seed coats, whereas it is easier for them to handle the smaller seeds of Ce. tomentosa. However, we found that A. peninsulae did not feed on the seeds of Ce. tomentosa, which could be because these seeds are too small to provide sufficient food resources.

According to the principle of competitive exclusion, competitors for the same limiting resource cannot coexist, but it is very difficult to directly observe competition in nature, particularly in the cases of interspecific and intraspecific competition in rodents. The food selection results of this study indicate that the four sympatric rodent species compete with each other for food and could have a high degree of niche overlap for the same food resources. However, this study did not account for factors such as differences in the levels of resource availability and competition, which are the outcome of long-term adaptation of the animals to their natural environment, and thus reflect their potential patterns of food resource niche differentiation. Niche differentiation avoids competition and enables sympatric species to coexist despite limited resources, thus enriching biodiversity and being necessary to sustain the coexistence of species (Kartzinel et al. 2015). Such niche differentiation also depends on the different habitats or microhabitats in which the animals live. Apodemus peninsulae is the dominant species in the broad-leaved coniferous and broad-leaved mixed forests in the north. Apodemus agrarius is primarily distributed in the purlieus of forests. Tscherskia triton occupies various habitats but dominates in grassland, farmland, and hilly areas, while Cl. rufocanus is primarily distributed in coniferous forest habitats. Moreover, feeding niche differentiation does not necessarily indicate the absence of competition, which is related to the amount of food resources. Abundant food resources enable greater interspecies niche overlap, whereas scarce food resources lead to competition (Lawlor 1980).

The characteristics of seeds and the intrinsic factors of the rodents exert important effects on the food selection. Rodents can identify different seed properties of the sympatric distribution and form specific feeding preferences. The four rodents all favored the seeds of Pi. koraiensis, Co. mandshurica, and Q. mongolica in a temperate forest in northeast China. Therefore, there are different degrees of overlap in food selection among the sympatric species of rodents because of different degrees of shared food preferences. In order to avoid excessive sympatric competition, rodents adjust their food preference strategies to differentiate feeding niches and thus achieve coexistence.

This research was funded by the Natural Science Foundation of Heilongjiang Province of China (SS2021C006), the Science Research Project of Mudanjiang Normal University (GP2021006), the Science Research Project of the Education Department of Heilongjiang Province (1451PT007). We are grateful to the people who helped collect behavioral data in Sandao forest farm. We thank the anonymous reviewers for their constructive comments on the manuscript. We thank Zhulin Han, Man Jiang, and LEXIS (Scientific editorial experts, United States, LEXIS Academic Service, LLC) for their linguistic assistance during the preparation of this manuscript.