Research Article |
Corresponding author: Dianwei Li ( swxldw@126.com ) Academic editor: Raquel López-Antoñanzas
© 2020 Dianwei Li, Jingwei Hao, Xu Yao, Yang Liu, Ting Peng, Zhimin Jin, Fanxing Meng.
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, Hao J, Yao X, Liu Y, Peng T, Jin Z, Meng F (2020) Observations of the foraging behavior and activity patterns of the Korean wood mouse, Apodemus peninsulae, in China, using infra-red cameras. ZooKeys 992: 139-155. https://doi.org/10.3897/zookeys.992.57028
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Apodemus peninsulae, a dominant rodent species in temperature forests of northeastern China, is a model animal to explore the ecological functions of reciprocal coevolution of animals and plants. From August to October 2016, 24 infra-red cameras were installed to study the feeding behavior and activity patterns of A. peninsulae in its natural environment. By analyzing 5618 video records, we found that feeding behavior, followed by motor and sentinel behaviors, was their main activity. In the behavior spectra, motor behavior (creep, walk, and skip), feeding behavior (forage, feeding, transport, hoarding, and clean), and sentinel behavior (alert, flee, banishment, and coexistence) accounted for 57.96%, 40.36%, and 1.68% of their behavior, respectively. The peak of feeding behavior occurred between 18:00 and 23:00, and feeding behavior frequency, duration, and activity rhythms differ among August to October. Furthermore, activity was the greatest after sunset and before sunrise, indicating a nocturnal lifestyle; however, from August to October, the start time of the activity was earlier, and the end time was later than usual. On average, mice spent 21.6 ± 11.6 times/night feeding, with a duration of 63.58 ± 98.36 s; while they spent less time in foraging, 39.05 ± 51.63 s. We found a significant difference in feeding and foraging frequency, with mice spending on average 10.84 ± 9.85 times/night and 9.23 ± 11.17 times/night, respectively. Our results show that feeding and foraging behavior is also influenced by light intensity, suggesting a preference for crepuscular periods of the day. Infra-red cameras are very useful in detecting activity patterns of animals that are not easily observable; these cameras are able to capture a large amount of valuable information for research into ecological functions.
Activity rhythm, feeding behavior, Glires, infra-red camera
Through adaptive evolution, animals respond to environmental factors, as well as their physiology, in order to adapt to their environment (
Foraging activity of animals involves a wide spectrum of behaviors used in the quest to find food. Foraging and feeding behaviors are often linked together, and animals will use a combination of strategies. Foraging and feeding behaviors include finding, obtaining, processing, ingesting, and hoarding, following specific pattern specific to the animal. Depending on the need, feeding can occur at the site where food is found or can be moved and consumed somewhere else. The decision to do so is dependent on external pressures such as predation, the time available for foraging, and environmental factors such as temperature (
Infra-red (IR) cameras have been found to be highly beneficial to ecological studies of cryptic animals, those that are active at night when it is difficult to see them, or those that occur in hard to reach locations. Moreover, IR cameras have many benefits, such as being non-invasive, capacity for long-term monitoring with 24 hour or longer monitoring (
The Korean wood mouse, Apodemus peninsulae, is a dominant species of the Glires community in temperate forests in northeastern China, inhabiting a variety of habitats such as forests, shrubs, glades, grasslands, and farmlands at the forest margins. This species feeds on and stores a variety of seeds and fruits from plants such as Quercus mongolican, Pinus koraiensis, and Corylus mandshurica (
The study was conducted from June 2015 to October 2016. The research site was in a forested area of Hengdaohezi town, Hailin City (44°44'N–44°55'N, 129°6'E–129°15'E, elevation 460–600 m), at the northern end of the Changbai Mountains in northeastern China, the east vein of the main ridge of Zhangguangcai Mountain. The mountain runs northwest-southeast. The climate is temperate continental monsoon, 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. About 100–160 days in the year are frost free. The first frost is in late September, and the last frost is in late April to early May. Precipitation is concentrated in June to September and varies between 400 mm and 800 mm. The forests in this area are dominated by secondary vegetation. There is a high abundance and diversity of Glires, largely dominated by combinations of various species such as A. peninsulae, A. agrarius, and Clethrionomys rufocanus.
In the theropencedrymion, three alternative plots with less human interference were selected for research. For each plot, we first used the rat traps method to investigate the presence of small Glires in the area. The plot with the largest capture rate of A. peninsulae was selected as the research site. The chosen site was 100 m × 150 m and at an altitude of 533–552 m.
In the study plot, four sample strips with an interval of 20 m were set, and six IR cameras (Ltl Acorn, LTL-6310MC) were installed in each sample strip. The IR camera interval was 20 m, with 24 cameras in total. The IR cameras were set to the photo + video mode. Each camera was set to take three shots after triggering and then to automatically record for 15 s after every 30 s interval. Cameras automatically recorded the date, time, environmental temperature, and other information. Cameras were fixed on tree trunks, or other fixed objects, about 30 cm above the ground, and baits (marked seeds of Quercus mongolican, Pinus koraiensis, and Corylus mandshurica) were placed on the ground approximately 30–80 cm in front of the camera. Ten days later, cameras were retrieved to collect and analyze the photos and videos.
Once the target animal was identified, the following observations were recorded, characterized, and later analyzed in order to construct the feeding and foraging behavior spectrum. The characterization included noting the type, frequency, and duration of behaviors exhibited during feeding and foraging. Due to the short duration of the video recording interval, 30 s, the video recording time, location of activity, and state of the target animal before and after the activity was used to assess whether the activity was continuous. The activity was considered to be continuous if the location and behavior did not change for the duration of the recording.
The environmental temperature was measured with the IR cameras, while light intensity was measured during early, middle, and late stage of the survey period, respectively. The measurements were taken once an hour only between 17:00 and 20:00 in the evening and 3:00 and 5:00 in the morning. For the sunrise and sunset time, we referred to local climate data and calculated the median.
The data was tested for normality and equality of variance using the Kolmogorov-Smirnov and Levene’s test of homogeneity. Data was treated with respective tests depending on whether they met or did not met the assumptions of normality. The Kruskal-Wallis H test (nonparametric test) was used to compare the significant differences in behavior frequency, behavior duration, temperature, and light intensity among the three months. The t-test (Parametric test) or Mann-Whitney U test (nonparametric test) was used to test the differences between the different months. The association between feeding frequency, light intensity, and temperature was tested using the Pearson Correlation analysis. All data were expressed as mean ± sd and statistical significance was accepted when α < 0.05. All statistical analyses were conducted in SPSS 22.0 software.
Among the 6383 effective recorded activities in the video, 5618 were of A. peninsulae, accounting for 85.73% of all the Glire species in the area. Other recorded Glires include Tamias sibiricus with 523 records, squirrel with 226 records, and Clethrionomys rufocanus with 16, accounting for 7.98%, 3.45%, and 2.84%, respectively. Therefore, A. peninsulae was the absolute dominant species in the selected research plot.
Apodemus peninsulae behavior was analyzed from the video records. The main behavior patterns are as follows:
A series of animal behaviors with obvious spatial displacements in different positions through various types of movement.
A series of behaviors exhibited by animals during feeding.
A series of behaviors of animals exhibited in response to risks and disturbances in the environment, and vigilance in response to what is in the environment to avoid being depredated.
The start and end time of activity was consistent with sunrise and sunset; the percentage of activity time of A. peninsulae after sunset and sunrise was 100%, and 99.96%, respectively. Only two observations of activities that extended past sunrise by 30 minutes were found (Table
The activity time of A. peninsulae and partial climatic characteristics.
Month | Earliest time | Latest time | Sunset time | Sunrise time | Temperature (°C) | Illumination (Lx) |
---|---|---|---|---|---|---|
8 | 19:08:48 | 04:02:09 | 18:40 | 4:18 | 19.1 ± 2.2 | 371.4 ± 938.9 |
(18:31–18:47) | (4:12–4:24) | |||||
9 | 17:21:37 | 05:54:53 | 17:19 | 5:12 | 10.0 ± 1.6 | 64.6 ± 138.5 |
(17:10–17:29) | (5:06–5:18) | |||||
10 | 17:00:46 | 05:31:10 | 16:46 | 5:34 | 4.3 ± 1.4 | 16.3 ± 38.4 |
(16:37–16:55) | (5:28–5:40) |
Forage, feeding, and transport in feeding behavior were the main activities of A. peninsulae and were accompanied with motor and sentinel behavior. Of the total number of records (4403) of various types of behaviors, 57.96% (2552) were motor, 40.36% (1777) were feeding, and 1.68% (74) were sentinel behaviors (Fig.
Feeding behavior frequency varied significantly in different months (H = 82.848, df = 2, P < 0.001). Total frequency was 21.6 ± 11.6 times/night (4.2–41.6 times / night, N = 26), of which 7.2 ± 2.8 times/night (4.2–10.5 times/night, N = 5) in August, 29.7 ± 7.8 times/night (17.9–41.6 times/night, N = 14) in September, which was the most frequent month, and 15.7 ± 7.5 times (4.5–25.4 times/night, N = 7) in October. The frequency of activities in August was significantly less than that in September (t = −9.220, P < 0.001) and October (t = −2.382, P < 0.05), and the frequency of activities in September was higher than October (t = 3.931, P < 0.01) (Table
Frequency and duration of feeding behavior of A. peninsulae in different months.
Month | Frequency(time/night) | Duration (s) | ||||
---|---|---|---|---|---|---|
Activity | Forage | Feeding | Transport | Forage | Feeding | |
8 | 7.2 ± 2.8 | 4.58 ± 2.87 | 4.17 ± 4.83 | 2.48 ± 1.86 | 42.78 ± 44.95 | 91.10 ± 118.02 |
9 | 29.7 ± 7.8 | 21.60 ± 10.02 | 12.30 ± 10.55 | 4.89 ± 5.90 | 47.05 ± 66.80 | 68.51 ± 102.98 |
10 | 15.7 ± 7.5 | 10.10 ± 8.36 | 11.35 ± 14.09 | 6.06 ± 4.83 | 29.16 ± 30.36 | 53.83 ± 88.72 |
Total | 21.6 ± 11.6 | 10.84 ± 9.85 | 9.23 ± 11.17 | 4.37 ± 4.57 | 39.05 ± 51.63 | 63.58 ± 98.36 |
The frequency and duration of three feeding behaviors were all different. The average frequency of forage, feeding and transport was 10.84 ± 9.85 times/night, 9.23 ± 11.17 times/night, and 4.37 ± 4.57 times/night, respectively. The frequency of forage was significantly higher than feeding and transport (H = 23.092, df = 2, P < 0.001). Only in September did the frequency of three behaviors show significant differences from August to October (H = 25.614, df = 2, P < 0.001) (Table
Our observations show that the peak of feeding behavior occurs between 18:00 and 23:00 and varies from month to month. In August, only a single feeding peak was observed which started after 19:00, peaking between 22:00 and 23:00, and reducing after 3:00. In September and October, the activity started after 17:00, peaking between 18:00 and 20:00, which was earlier than that in August. In addition, the frequency of feeding was significantly higher than that in August, after 20:00, with a smooth curve and began to decrease after 4:00 (Fig.
A. peninsulae showed a highest activity frequency on the first day it encountered a food source, with an average of 32.7 ± 7.1 times/night, then followed by daily feeding frequency between 10 and 22 times. This trend varied from month to month, with the feeding peak in August and decreasing thereafter. The feeding frequency showed the highest peaks on days 1, 4, 7, and 9 in September, and on days 1, 8, and 10 in October (Fig.
From August to October, the temperature and light intensity decreased month by month. The temperature (H = 223.041, df = 2, P < 0.001) and light intensity (H = 14.812, df = 2, P < 0.001) from August to October showed significant differences. There was a strong positive association between temperature and feeding behavior during the month of September (R = 0.361, P < 0.001), but not during August and October (August: R = 0.118, P > 0.05; October: R = −0.036, P > 0.05; Fig.
Apodemus peninsulae spends the majority of its active time feeding and exhibits some motor behaviors and sentinel behaviors during feeding. Our results show that foraging was the most frequent behavior and feeding was the longest behavior. A. peninsulae usually fed in situ when first encountering seeds, then transported seeds for later feeding or storage. The animals compensated for energy loss by reducing the frequency of foraging activity and spending more time to increase other activities such as sentinel behaviors so that they were more vigilant. Due to the limitation of the monitoring range of the camera, we were unable to follow post-transport feeding and hoarding activities, leading to an inaccurate calculation. We had similar results to
Feeding and transport in A. peninsulae play two completely opposite roles in vegetation regeneration. On the one hand, feeding on a large number of seeds is harmful to forest regeneration (
Activity rhythm is a comprehensive adaptation to obtain the greatest survival benefits under various conditions and is affected by a variety of internal and external factors. Among them, solar radiation, light intensity, and environmental temperature are the main factors that affect animal activity rhythm (
Temperature is known to have considerable effect on changes in the daily activity rhythm in animals (
Studies under laboratory conditions have shown that A. peninsulae can be active both day and night in the spring (May), and the activity duration at night is more than that in day (
IR cameras have been used to assess species diversity survey and population density estimation in large mammals (
Infra-red cameras were used to record in natural conditions the feeding behavior of a small species of Glires, A. peninsulae, with both nocturnal and crepuscular behavior. In the behavior spectra, feeding behavior followed by motor and sentinel behaviors were the main activities of this species. It spent the majority of its active time feeding and foraging. The behavior was influenced by light intensity, suggesting a preference for crepuscular periods of the day. This species’ activities had significant seasonal differences and is seen as an adaptation strategy in response to seasonal changes in food and the environment. Our results show that IR cameras are highly useful in ecological studies of species of Glires that are not easily observable. IR cameras are able to capture much valuable information on ecological functions.
We are grateful to the people who helped install infra-red cameras and collect behaviorial data in Hengdaohezi. We thank the anonymous reviewers for their constructive comments on the manuscript. This research was funded by the Science Research Project of the Education Department of Heilongjiang Province (1353ZD005), the Innovation Research Project of Mudanjiang Normal University (GP2019004), and the Doctoral Research Fund of Mudanjiang Normal University (MNUB201907).