Coexistence of roof rats and carnivores in barns on a livestock farm in Japan
Abstract
Brown rats (Rattus norvegicus), roof rats (Rattus rattus), and house mice (Mus musculus) are considered to be important pests on livestock farms. Although the diel activity patterns of rodents are key to their control, information on this aspect of their ecology is limited. Furthermore, the effect of carnivores on rodent activity patterns as well as the carnivore species present on livestock farms is unclear. Here, we set camera traps in an open-type cow barn and in an enclosed pig barn on the same livestock farm in Japan from August through October 2021. The only rodents observed in both barns were roof rats, and the carnivore species observed were dogs (Canis familiaris), cats (Felis catus), and Japanese weasels (Mustela itatsi). Roof rats showed different patterns of activity and behavior between the barns. However, because the pattern in both barns was nocturnal, the activity patterns of roof rats and carnivores showed a moderate to high degree of overlap. Therefore, roof rats did not appear to shift their activity patterns to avoid nocturnal carnivores. Taken together, the present study provides valuable information for rodent control on livestock farms in Japan.
1 INTRODUCTION
Brown rats (Rattus norvegicus), roof rats (Rattus rattus), and house mice (Mus musculus) are three of the most important pest rodent species not only in urban centers (Himsworth et al., 2013) but also on livestock farms (Leirs et al., 2004). Although the diel activity patterns of rodents are key to their control, information on this aspect of their ecology is limited. Several attempts have been made to analyze the intrinsic activity patterns of brown rats (Calhoun, 1962; Klemann & Pelz, 2006; Takahashi & Lore, 1980), roof rats (Salgado et al., 2022; Tanikawa, 1995), and house mice (Daan et al., 2011; Robbers et al., 2015). However, these studies paid little attention to the effects of predators living in the same habitat. Brown rats have been shown to exhibit an altered activity pattern to avoid carnivores (Fenn & Macdonald, 1995; Parsons et al., 2018). Therefore, it is more appropriate to understand the diel activity patterns of pest rodents in the context of interactions with other carnivore species present on livestock farms.
It has been reported that a wide variety of carnivore species visit livestock farms, ranging from wild canids (African wild dogs, black baked jackals, coyotes, gray wolves, spotted hyenas, and wolves), ursids (American black bears, Asiatic black bears, brown bears, and grizzly bears), and felines (e.g., caracals, cheetahs, Eurasian lynxes, jaguars, leopards, lions, pumas, snow leopards, and tigers) (Gehring et al., 2010; Miller, 2015; Miller et al., 2016). However, with the exception of Asiatic black bears and brown bears, these carnivores are not found in Japan. In contrast, dogs (Canis familiaris) and cats (Felis catus) are known to be the most populous free-ranging carnivores in areas close to human society (Cecchetti et al., 2021; Hughes & Macdonald, 2013). In fact, from April 1, 2022 to March 31, 2023, 19,816 unowned dogs and 20,842 unowned cats were sheltered in Japan (Ministry of the Environment, 2024). Based on these facts, we hypothesize that dogs and cats are two major carnivores visiting barns on livestock farms in Japan and that rodents shift their activity patterns to avoid these nocturnal carnivores.
To assess these hypotheses, we set up camera traps in a dairy cow and a breeding pig barn on the same livestock farm in Japan from August through October 2021. We identified the rodent species present and the carnivore species that visited these barns and analyzed their diel activity patterns. We also analyzed their behavior on video. We then evaluated the overlap between the activity patterns of rodents and carnivores.
2 MATERIALS AND METHODS
This study was an observational study using camera traps, and as such, the National Agriculture and Food Research Organization Research Ethics Committee judged that it does not require ethical approval.
2.1 Location
The study was conducted on a livestock farm in Kasama, Ibaraki Prefecture, Japan (36°16′28.7″ N, 140°19′46.4″ E). It was located on a busy road with a restaurant (500 m), a gas station (500 m), a barber shop (650 m), two convenience stores (900 and 1000 m), a highway interchange (900 m), a café (1000 m), and many residences and sales offices nearby. In addition, the total length of roads within a 5-km radius was 513 km, which is longer than the areas considered to be peri-urban in a previous study (between 140 and 440 km) (Williams et al., 2005).
The dairy cow barn (approximately 20 × 31.5 m) was an open-type barn with a vented gable roof. There were two walls on two short sides of the barn. During the camera trapping, the barn housed 15 cows in tie stalls. When calves were born, they were housed individually in small pens. The cows were fed straw, grass and corn silage, and commercial concentrates once in the morning and once in the afternoon. The breeding pig barn (approximately 8.1 × 33 m) was an enclosed barn with a vented gable roof. There were four walls, one on each side of the barn. Inside the barn, three large (approximately 3.8 × 6.1 m) and six small (approximately 3.6 × 2.7 m) pens were aligned along one long side of the barn, all of which were connected to individual outdoor pens by a small door. The outdoor pens were enclosed with wire mesh. Two to three adult sows were housed in each of the three large pens. When piglets were born, four to six pigs were housed in each of the two small pens until shipment. The pigs were fed a commercial feed formulation once in the morning and once in the afternoon. The distance between the cow and pig barns was approximately 165 m, with several paths and buildings between them. Before the experiment, we confirmed that there were no carnivore nests in the barns and on the farm.
2.2 Camera trapping from August 13 to October 20, 2021
We set up 11 and 13 cameras by wrapping wires around the posts in the cow and pig barns, respectively. These cameras were sufficient to monitor the entire area of each barn. We used Hyke Cam LT4G cameras (Hyke Inc., Hokkaido, Japan), which were equipped with a passive, movement-triggered infrared sensor. A 60-s video was recorded with no interval and high sensor sensitivity when animal movement was detected within the range of the sensor. Under low-light conditions, the cameras used an infrared light during recording. Experimenters entered the barns only to check the camera batteries and memory cards every 2 weeks to minimize disturbance. Each camera was kept in only one location during the study. No humans appeared in the barns except for the caretakers.
2.3 Data analysis
Because the number of videos was too small to analyze cats, dogs, and Japanese weasels separately, these three species were combined into one group (carnivores). We defined 05:00–17:59 h as daytime and 18:00–04:59 h as nighttime based on sunrise and sunset during this period reported on the Japan Meteorological Agency website. The ratio of videos recorded during the night with respect to all videos (night ratio) was calculated in each barn. To analyze the diel activity patterns, we estimated the probability density of target animals by kernel density estimation using the “Overlap” package (Meredith et al., 2024) of R 4.2.2 (R Core Team, 2024). To analyze the overlap between the two probability densities, we calculated the overlap coefficient (Δ) and 95% confidence interval using the same package. Here, we used 1 and 4 in accordance with a previous study (Ridout & Linkie, 2009) when the number of videos was less than 75 and more than 75, respectively. The overlap was considered to be low (Δ < 0.5), moderate (Δ 0.5–0.75), or high (Δ > 0.75) (Monterroso et al., 2014; Perez-Irineo et al., 2021). Confidence intervals were obtained from 1000 bootstrap samples.
We recorded the occurrence of exploration (rearing or sniffing an object), veering (changing direction), social behavior (any physical touching of other rodents), resting (lying on its stomach or its side), grooming (face washing, oral grooming, and scratch grooming), and stretch attend posture (SAP, approaching an object with a flattened body with its head oriented toward the object) exhibited by rodents and carnivores in each video. The occurrence of hunting (both rodents and carnivores were recorded, and the carnivores chased the rodents) was also recorded. The percentage of videos that included each behavior with respect to all videos was calculated in each barn.
3 RESULTS
In this study, we obtained 17,003 videos. Among them, the only rodents we observed were roof rats (12,830 videos), and no videos showed brown rats or house mice. Carnivores that regularly visited these barns were five dogs (67 videos) and two cats (129 videos), which were identified based on body size and appearance (Figure S1). In addition, a Japanese weasel (Mustela itatsi) was once observed in the pig barn (1 video) (Figure S1). The cameras also recorded the livestock caretakers (3970 videos). The RAI of these animals is shown in Table 1.
| Cow barn | Pig barn | |
|---|---|---|
| Rodents (total) | 75 | 160 |
| Roof rats | 75 | 160 |
| Brown rats | 0 | 0 |
| House mice | 0 | 0 |
| Caretakers | 73 | 59 |
| Carnivores (total) | 14 | 8.3 |
| Cats | 7 | 8 |
| Dogs | 7 | 0 |
| Japanese weasels | 0 | 0.3 |
The probability densities and behaviors are shown in Figure 1. In the cow barn (Figure 1a), the probability density of roof rats showed a unimodal pattern. Most of the videos were recorded during the night (night ratio = 0.99). Roof rats showed 553 behaviors in 417 videos. The observed behaviors, in order of frequency, were exploration (50.7%), veering (37.9%), social behavior (7.4%), resting (1.6%), grooming (1.3%), and SAP (1.1%). The probability density of carnivores showed a bimodal pattern. Most of the videos were recorded during the night (night ratio = 0.93). Carnivores showed 56 behaviors in 53 videos. The observed behaviors were exploration (91.1%), veering (5.4%), grooming (1.8%), and SAP (1.8%). In the pig barn (Figure 1b), the probability density of roof rats showed a bimodal pattern. More videos were recorded at night than during the day (night ratio = 0.64). Roof rats showed 1455 behaviors in 1063 videos. The observed behaviors were social behavior (31.1%), exploration (26.0%), grooming (25.0%), resting (15.7%), veering (1.3%), and SAP (0.9%). The probability density of carnivores showed a unimodal pattern. More videos were recorded at night than during the day (night ratio = 0.86). Carnivores showed 28 behaviors in 23 videos. The observed behaviors were exploration (57.1%), grooming (28.6%), resting (7.1%), and hunting (7.1%). It should be noted that no hunting resulted in preying. In addition, in both barns, there was no video showing carnivores entering the barns with the caretakers.
We also observed the feeding behavior of roof rats and carnivores. In the cow barn, roof rats consumed concentrates scattered on the floor. Although this was clearly observed when it occurred in the immediate area of the cameras, the videos were not clear enough to quantify it in more distant areas. Dogs (10 videos) and cats (1 video) also consumed concentrates on the floor. In the pig barn, caretakers frequently observed roof rats consuming concentrates in the feeders. However, although we observed many roof rats in the feeders, we were unable to quantify consumption because all the feeders were in distant areas from the cameras. There were no videos of dogs or cats consuming concentrates in the feeders.
The overlap between the densities is shown in Figure 2. The probability density of roof rats was highly overlapped with that of carnivores in the cow barn (Figure 2a, Δ = 0.82, CI: 0.76–0.90) and moderately overlapped with that of carnivores in the pig barn (Figure 2b, Δ = 0.60, CI: 0.53–0.67). In addition to the carnivores, the livestock caretakers also routinely visited both the cow and pig barns. When we evaluated the overlap, the probability density of caretakers showed a limited overlap with that of roof rats in the cow barn (Figure S2a, Δ = 0.01, CI: 0.01–0.02) and in the pig barn (Figure S2b, Δ = 0.27, CI: 0.26–0.28).
4 DISCUSSION
In the present study, the only rodents we observed in both barns were roof rats. Although cats were observed in similar numbers between the barns, dogs and Japanese weasels were observed only in the cow barn and pig barn, respectively. We also found that the overlap in the activity patterns of roof rats and carnivores was moderate to high in both barns. Therefore, roof rats did not appear to shift their activity patterns to avoid nocturnal carnivores. Taken together, the present study provides valuable information for rodent control on livestock farms in Japan.
Because our data are limited, it is worthwhile to consider limitations. First, the present findings may be affected by the season. Brown rats and/or house mice may be observed in other seasons. In addition, cold weather in winter and estrus in spring and fall would increase the amount of time carnivores spend in the barns, which may alter the activity pattern of roof rats. However, the season would not affect the foraging behavior of the carnivores because they can consume livestock concentrates throughout the year. Second, the present findings may be specific to this farm. However, this seems less likely because small carnivores have been observed even in the windowless poultry barns on many farms in Japan (Yamaguchi, 2019).
This is the first report to show that dogs and cats are two major carnivore species visiting livestock farms in Japan. Analysis of their RAI suggests that cats and Japanese weasels can easily enter enclosed barns. As a part of the classical swine fever defense (Meng et al., 2009; Shimizu et al., 2021), the barn was surrounded by a wire fence. In addition, the barn and outdoor pens were completely enclosed in wire mesh. Nevertheless, the RAIs of the cats were similar between the enclosed pig barn and the open-type cow barn. Furthermore, Japanese weasels were only observed in the pig barn. In addition to dogs and cats, mammals such as raccoons (Procyon lotor), raccoon dogs (Nyctereutes procyonoides), and Japanese hares (Lepus brachyurus) are also known to be in urban areas of Japan (Saito & Koike, 2013). Therefore, in addition to livestock, such mammals should be considered when implementing rodent control campaigns, even in enclosed barns.
We also reported for the first time the diel activity patterns of roof rats living in livestock barns. We found that the activity patterns differed between the cow and pig barns. However, contrary to our hypothesis, the probability density of roof rats overlapped moderately to highly with that of the carnivores. Therefore, it is possible that the carnivores, especially cats, do not pose the same degree of threat to roof rats as they do to brown rats. Roof rats are usually active on the higher levels, such as the roof, beams, and girders of barns. Even when they come down to the ground, they can easily climb up vertical columns (Ewer, 1971; Tanikawa & Sato, 1993) and return to the higher levels. In contrast, cats, dogs, and Japanese weasels are mostly active on the ground level, although cats and Japanese weasels can climb up to a certain level, including on shelves or steps on walls. Therefore, unlike brown rats, which are mostly active at ground level, roof rats do not necessarily need to perceive these carnivores as risks when they enter barns at ground level. Indeed, in our videos, the roof rats stayed on the beams or in the ceiling insulation, even when a cat was watching them from the top of a pig pen wall (Figure 3). A previous study reporting that roof rats did not avoid cat and dog odors (Carthey & Banks, 2018) further supports this possibility.
In summary, we found the coexistence of roof rats and carnivores during the night in barns on the livestock farm in Japan. On the basis of these findings, we recommend that rodent control campaigns be implemented at night in barns where roof rats are present. However, even in enclosed barns, it should be assumed that small wildlife species will be present during the campaign, in addition to the housed livestock. Further analysis of the ecology of rodents in livestock barns would contribute to the improvement of public health and animal health by effectively preventing food-borne zoonoses and disease infections in livestock.
ACKNOWLEDGMENTS
This study was supported by JSPS KAKENHI (grant numbers 20H03160 and 22K14979). We would like to thank Dr. Kuwahara and all the staff of the Animal Resource Science Center, The University of Tokyo for their kind support.
CONFLICT OF INTEREST STATEMENT
The authors declare no conflict of interest for this article.
