Research Article |
Corresponding author: Dianwei Li ( swxldw@126.com ) Corresponding author: Zhimin Jin ( swxjzm@126.com ) Academic editor: Nilton Cáceres
© 2021 Dianwei Li, Yang Liu, Hongjia Shan, Na Li, Jingwei Hao, Binbin Yang, Ting Peng, Zhimin Jin.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Li D, Liu Y, Shan H, Li N, Hao J, Yang B, Peng T, Jin Z (2021) Effects of season and food on the scatter-hoarding behavior of rodents in temperate forests of Northeast China. ZooKeys 1025: 73-89. https://doi.org/10.3897/zookeys.1025.60972
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To explore the differences in hoarding strategies of rodents for different seeds in various seasons, we labeled and released the seeds of Pinus koraiensis, Corylus mandshurica, Quercus mongolica and Prunus sibirica in temperate forests of Northeast China and investigated the fate of the seeds in spring and autumn. The analysis showed that the hoarding strategies of the rodents varied substantially between seasons. The seeds were consumed faster in the spring than in the autumn. More than 50% of the seeds in the two seasons were consumed by the 16th day. It took 36 days to consume 75% of the seeds in the spring and 44 days in the autumn. The rate of consumption of the seeds in the spring was greater than in the autumn, and the rate of spread of the seeds was greater in the autumn. The distances of removal for the consumption and dispersal of seeds in the spring (3.26 ± 3.21 m and 4.15 ± 3.52 m, respectively) were both shorter than those in the autumn (3.74 ± 3.41 m and 4.87 ± 3.94 m, respectively). In addition, the fate of different seeds varied significantly owing to differences in hoarding strategies. The seeds of the three preferred species, P. koraiensis, C. mandshurica, and Q. mongolica, were quickly consumed. More than 90% of the seeds of these species were consumed. Only 21% of Pr. sibirica seeds were slowly consumed, and the two seasons had the same seed consumption rate patterns: the consumption rate of P. koraiensis seeds was the highest, followed by C. mandshurica, then Q. mongolica, and finally Pr. sibirica. The median removal times of the two seasons were different, but the rules were the same: P. koraiensis was the shortest, followed by C. mandshurica, and the third was Q. mongolica. In both seasons, the most predated in situ seeds were those of P. koraiensis; the most hoarded seeds were those of C. mandshurica, and the most unconsumed seeds were those of Pr. sibirica.
Murids, rodents, scatter-hoarding, seed fate, seed dispersal, voles
Rodents play an important role in the process of plant seed dispersal and regeneration (
The hoarding behavior of rodents is a special type of feeding behavior; it is a vital adaptive strategy for many rodents during periods of food scarcity (
The Northeast China temperate zone is rich in forest vegetation resources and is an important resource of species and bank for seeds. Rodents not only damage forest resources by their predation on vegetation and seeds, but also promote the regeneration of vegetation by scatter-hoarding food (
The study was conducted from April to November, 2018. The research site was located in a forested area of the Sandao Forest Farm (44°40'N–44°45'N, 129°24'E–129°32'E, elevation 380 to 550 m), Mudanjiang City, located at the northern end of the Changbai Mountains in northeastern China, the east vein of the main ridge of the Zhangguangcai Mountain. The climate is a temperate and cold continental monsoon climate with four distinct seasons and a hot rainy season. The maximum temperature is 37 °C. The minimum temperature is -44.1 °C, and the annual average temperature is 2.3–3.7 °C. Approximately 100–160 days in the year are frost free. The first frost in most areas appears is in late September, and the last frost is in late April to early May. Precipitation is concentrated in June to September and varies from 400 mm to 800 mm.
The experiment was conducted in secondary coniferous and broad-leaved mixed forest that had been least disturbed. Common canopy tree species included P. koraiensis, Q. mongolica, Larix gmelinii, Picea koraiensis, Abies nephrolepis, Betula platyphylla, Tilia amurensis, T. mandshurica, Juglans mandshurica, while the brush included primarily C. mandshurica, Lonicera maackii, Acanthopanax senticosus, Trichosanthes kirilowii, and Syringa reticulata. The rodents in forests were highly abundant and diverse, largely dominated by different combinations of species, with Apodemus peninsulae, A. agrarius, and Clethrionomys rufocanus being the dominant species.
Healthy seeds of P. koraiensis, C. mandshurica, Q. mongolica, and Pr. sibirica that had been selected in the field study experiment were tagged using an electric drill whose bit is 0.5 mm in diameter, to make a hole at one end of the seed. A thin red plastic sheet was cut into a 3 cm × 1 cm rectangular plastic plate (
Food release stations in the forest were randomly arranged and spaced more than 50 m apart. Each release station released 20 seeds of each type for a total of 80. There were 15 release stations in the spring with 300 seeds of each type, totaling 1200. There were 9 release stations in the autumn with 180 seeds of each type, totaling 720.
The study was conducted on days 1, 2, 3, 4, 6, 8, 12, 16, 20, 28, 36, 44, and 60 after release. The fate and characteristics and dispersal distance of the seeds were measured.
The fate of the seeds released in the field experiment is defined as follows (
1. Intact in situ (IS): seeds not eaten or removed from the station
2. Predation in situ (PS): seed kernels eaten at the seed station
3. Predation after removal (PR): seed kernels eaten after removal
4. Intact after removal (IR): seeds not eaten and abandoned on the surface of ground after removal
5. Hoarded after removal (HR): seeds buried in the soil or humus layer after removal
6. Missing after removal (MR): seeds removed but not found
7. Consumption: With the exception of IS seeds, the fate of other seeds is defined as consumption by rodents.
8. Predation: PS and PR are defined as predation (PS + PR)
9. Dispersal: IR, HR, and MR are defined as dispersal. However, there were no data records for the survey indicators of the missing seeds, so they could not be calculated during the inspection and comparison (IR + HR + MR)
10. Median removal time (MRT) of the seeds: the time at which 50% of the seeds were removed (expressed in days), which was used to compare the seed removal rates in both types of vegetation.
All statistical analyses were conducted in SPSS 22.0 for Windows (IBM, Inc., Armonk, NY, USA). Before the data analysis, the data was tested for normality and equality of variance using the Kolmogorov-Smirnov and Homogeneity-of-variance tests. Data were treated with respective nonparametric tests depending on whether they met the assumptions of normality. A Cox regression was used to analyze the seed survival rates, factoring in both seasons’ type and seeds. The Kruskal–Wallis H test (nonparametric) was used to compare the significant differences among the four seed species. The Mann–Whitney U test (nonparametric) was used to test the differences between the different seasons and different seed species. The data are represented as the mean ± SD. The values are considered statistically significant at P < 0.05.
According to the analysis of the seed survival curve (Fig.
According to the analysis of seed survival curves in different seasons (Fig.
According to the analysis of survival curves of four types of seeds in the spring and autumn (Fig.
There were no differences in the average time of the earliest food discovery between the two seasons (Z = -0.508, P > 0.05). After the animals found the seeds, they chose different ones based on their preferences and performed different operations, resulting in various fates of the seeds. The sequences of the earliest consumption time of seeds in the spring and autumn were both as follows: C. mandshurica was the earliest, followed by P. koraiensis, then Q. mongolica, and finally Pr. sibirica. There were no differences in the earliest consumption time among P. koraiensis, C. mandshurica, and Q. mongolica in different seasons (spring: χ2 = 1.140, P > 0.05; autumn: χ2 = 0.634, P > 0.05). The earliest time of consumption of Pr. sibirica was significantly later than that of the other types of seeds in the spring and autumn (all P < 0.05) (Table
The earliest discovery time and consumption time of the different seeds in spring and autumn in temperate forests of Northeast China. The different superscript letters represent significant differences from each other (P < 0.05), based on Mann–Whitney U testing differences in the earliest discovery time between the spring and autumn, based on Kruskal–Wallis H testing differences in the earliest consumption time among the four seed species.
Season | Earliest discovery time (range; day) | Earliest consumption time (range; day) | |||
---|---|---|---|---|---|
P. koraiensis | C. mandshurica | Q. mongolica | Pr. sibirica | ||
Spring | 7.2 ± 8.8 (1–36)a | 10.7 ± 13.8 (1–60)b | 9.4 ± 13.0 (1–60)b | 9.6 ± 7.9 (1–60)b | 75.4 ± 38.1 (6–108)c |
Autumn | 5.8 ± 3.8 (2–12)a | 10.3 ± 8.1 (2–28)b | 9.1 ± 7.87 (3–28)b | 11.1 ± 7.0 (4–20)b | 70.7 ± 33.9 (12–92)c |
When the seed species were not distinguished, the MRT was around the 16th day. Seventy percent of the seeds were consumed at approximately the 36th day, and 18.08% of the seeds were still unconsumed after the 90th day (Fig.
Median time of removal of the different seeds in spring and autumn in temperate forests of Northeast China. The same superscript letters represent nonsignificance (P > 0.05), based on Mann–Whitney U testing differences in MRT between the spring and autumn, based on Kruskal–Wallis H testing differences in MRT among the three seed species.
Season | Median removal time (day) | |||
---|---|---|---|---|
P. koraiensis | C. mandshurica | Q. mongolica | Pr. sibirica | |
Spring | 13.6 ± 12.9a | 14.4 ± 14.0a | 18.5 ± 10.1a | – |
Autumn | 10.3 ± 8.1a | 13.8 ± 7.0a | 18.7 ± 12.4a | – |
Less than 100% of the seeds were consumed during the study. Therefore, the average removal time of the three types of seeds (P. koraiensis, C. mandshurica and Q. mongolica) was estimated based on the survey data of the seed station after predation (Table
The latest consumption time of the different seeds in spring and autumn in temperate forests of Northeast China. The different superscript letters represent significant differences from each other (P < 0.05), based on Mann–Whitney U testing differences in the latest consumption time between the spring and autumn, based on Kruskal–Wallis H testing differences in the latest consumption time among the three seed species.
Season | The latest consumption time (range; day) | |||
---|---|---|---|---|
P. koraiensis | C. mandshurica | Q. mongolica | Pr. sibirica | |
Spring | 18.3 ± 12.5(2–60)a | 22.1 ± 17.0(4–76)ab | 28.5 ± 17.7(12–76)b | – |
Autumn | 17.3 ± 7.2(8–28)a | 24.0 ± 12.8(4–44)a | 46.7 ± 17.9(28–76)b | – |
Different seeds had varied fates, and the seasonal differences in the seed fates were significant. More seeds were consumed in the spring than in the autumn. With the exception of Pr. sibirica seeds, the rates of consumption of the seeds of the other three species all exceeded 90%. In the spring, the rate of consumption of P. koraiensis seeds reached 99.56%, C. mandshurica seeds 100%, and Q. mongolica seeds 92.35%. In the autumn, the rate of consumption of P. koraiensis seeds reached 99.44%, C. mandshurica seeds 99.44%, and Q. mongolica seeds 97.22%. The rates of consumption of Pr. sibirica seeds in the spring and autumn were 21.0% and 3.33%, respectively (Fig.
In the spring, the proportions of seeds that were intact in situ (IS), predation in situ (PS), predation after removal (PR), intact after removal (IR), hoarded after removal (HR), and missing after removal (MR) were 14.20%, 41.52%, 13.59%, 1.45%, 11.07% and 18.17%, respectively. In the autumn, the proportions of seeds with corresponding fates were 25.14%, 8.47%, 7.92%, 5.28%, 19.58% and 33.61%, respectively (Fig.
The total predation rate of seeds was higher in the spring (55.11%) than in the autumn (16.39%). The total seed dispersal rate of seeds was higher in the autumn (58.47%) than in the spring (30.69%) (Fig.
The transport distances of seeds by PR in the spring and autumn were 3.26 ± 3.21 m and 3.74 ± 3.41 m, respectively, with no significant difference (Z = -1.276, P = 0.202 > 0.05).
The three species of seeds P. koraiensis (3.51 ± 3.25 m in the spring, 3.30 ± 2.03 m in the autumn), C. mandshurica (3.17 ± 2.91 m in the spring, 3.88 ± 2.19 m in the autumn), Q. mongolica (2.72 ± 3.37 m in the spring, 3.74 ± 3.76 m in the autumn) showed no seasonal differences in the transport distances of PR. Pr. sibirica seeds (7.73 ± 3.36 m in the spring) showed no PR of data records during the autumn study.
The seed dispersal distances in the spring and autumn were 4.15 ± 3.52 m and 4.87 ± 3.94 m, respectively, and the dispersal distance in the spring was significantly shorter than that in the autumn (Z = -2.008, P < 0.05). The dispersal distance of P. koraiensis seeds was significantly greater than that of the other three types (χ2 = 24.975, P < 0.001), and there was a difference between the other three types (all P > 0.05). The dispersal distance of P. koraiensis seeds in the spring (3.89 ± 2.05 m) was significantly shorter than that in the autumn (7.97 ± 5.33 m) (Z = -3.762, P < 0.001). C. mandshurica seeds (4.42 ± 3.72 m in the spring, and 4.12 ± 2.49 m in the autumn) , Q. mongolica seeds (6.16 ± 6.27 m in the spring, 3.69 ± 3.31 m in the autumn) and Pr. sibirica seeds (2.29 ± 1.50 m in the spring, 3.18 ± 2.66 m in the autumn) showed no seasonal differences in the diffusion distances (all P > 0.05). The dispersal distances of seeds were greater than the transport for predation distances (all P < 0.05).
Some studies have shown that feeding and hoarding behavior of rodents had significant seasonal differences and were seen as an adaptation strategy in response to seasonal changes in food and the environment in Northeast China (
In response to the seasonal changes and the impacts on food resources, coupled with the north temperate climate, some rodents showed different requirements to meet different life activities at different times (
Earlier results indicated that environment temperature has an important effect on changes in the activity behavior in rodents, with rodent species adjusting their foraging times and activities in response to changes in temperature (
The differences in seed characteristics and the animal’s needs will affect the hoarding behavior of animals, which manifests as preference for food selection (
Rodents change their predation and hoarding behavior strategies based on different seasons and foods. These animals adopt different foraging strategies so that the consumption of seeds has obvious seasonal differences. Food resources are scarce in the spring, and rodents spend more time foraging than in the autumn. Spring seeds are consumed in greater numbers and more quickly than in the autumn. In the spring, to meet the immediate demand for a supply of energy, rodents predate on more seeds. In the autumn, the abundance of seeds increases. To ensure the necessary food demand for winter survival, rodents disperse more seeds to different locations for hoarding, and the dispersal distance is relatively larger. For different seeds distributed in the same region, rodents will identify and judge the characteristics of the seeds, resulting in various fates for the seeds. Handling seeds in different ways leads to obvious predation preferences, and usually seeds that are rich in nutrients and easily handled are prioritized. Seeds with hard and thick seed coats are hoarded the most intensively.
This research was supported by the Innovation Research Project of Mudanjiang Normal University (GP2019004), the Natural Science Foundation of Heilongjiang Province of China (LH2020C071), the Doctoral Research Fund of Mudanjiang Normal University (MNUB201907) and the Undergraduate Innovation and Entrepreneurship Training Program (202010233012). We thank Zhulin Han, Man Jiang and LEXIS (Scientific editorial experts, United States, LEXIS Academic Service, LLC) for its linguistic assistance during the preparation of this manuscript.