In Japan, crop damage attributable to wildlife in 2021 was estimated to contribute to losses of $103 million (calculated by a rate of 150 yen per dollar), of which 39% was caused by sika deer (Cervus nippon) (Ministry of Agriculture, Forestry and Fisheries 2023). In recent years there has been an escalation in the severity of the damage. Sika deer graze the grasslands on livestock farms at high densities throughout the year (Kawamura et al. 2013; Nakamura et al. 2019), thereby adversely affecting grass yields (Nakamura et al. 2022b). These deer not only cause substantial economic losses by reducing forage crops, but also heighten the risk of infectious disease transmission through their contact with livestock. To mitigate the conflict between wild animals and human activities, a strategy to prevent the invasion of sika deer into agricultural fields is crucial. In this regard, protective fences, which are physical barriers, and electric fences, which are psychological deterrents, are commonly used to prevent the encroachment of sika deer. However, if mismanaged, these fences can become increasingly less effective over time. Indeed, wild animals are known to readily exploit gaps at the base of protective fences and between the wires of electric fences (Takayama et al. 2017). These errors are the result of human misunderstanding of the behavioral characteristics, learning, and sensory abilities of animals.

To effectively navigate complex environments, deer typically utilize their sense of sight to confirm the stimuli detected by their other senses (VerCauteren and Pipas 2003). Vision is characterized by visual acuity, color vision, and the visual field, and in this regard, the findings of some behavioral studies have indicated that sika deer can distinguish between several chromatic colors (Nakamura et al. 2018) and gray (Takayama et al. 2018), regardless of light conditions. However, Okubo et al. (2022) have established that these deer are unable to discriminate between specific color combinations (e.g., blue and purple-blue or blue and red-purple). Nevertheless, to the best of our knowledge, there have been no studies to date that have assessed the visual acuity of sika deer, and the extent to which they acquire visual information relating to objects, gaps between objects, and shapes has yet to be established.

To enhance animal management, the visual acuity of ungulate livestock species has previously been investigated to assess their sensory capabilities. For instance, Manda et al. (1993) and Tanaka et al. (1998) have demonstrated that visual acuity can be estimated in cattle (Bos taurus) and pigs (Sus scrofa domesticus) by means of operant learning experiments using Landolt rings as visual targets. These findings, combined with the color recognition abilities of cattle (Manda et al. 1989a, 1989b) and wild boars (S. scrofa) (Eguchi et al. 1997), have led to improvements in visual factors such as wire width and color, and have been shown to be applicable to behavior management using electric fences. From the visual acuity of sika deer, it is possible to estimate the degree to which they recognize fences before passing through them, providing important basic data for improving existing fences and developing new countermeasures. Accordingly, in this study, we similarly sought to determine the visual acuity of sika deer based on operant conditioning using Landolt rings. The primary aim of this study was to yield basic knowledge of sika deer vision. These insights could be channeled toward the creation of methods to control sika deer (in the context of them being agricultural pests).

Materials and methods

All experimental and animal care procedures were performed based on the protocols outlined in “The Guide for Care and Use of Laboratory Animals at Kagoshima University″. The study was conducted from June–October 2018 in a specially designed experimental enclosure (800 × 400 × 230 cm; Fig. 1) located on a private farm in Kagoshima, Japan. As test animals, we used two sika deer (C. nippon nippon; one male and female), each estimated to be approximately two years old, which were captured at the Iriki Farm, Faculty of Agriculture, Kagoshima University in October 2016, with permission from Kagoshima Prefecture (permission for wildlife capture under Article 9, Paragraph 1 of Wildlife Protection, Control, and Hunting Management Act, No. 88 by Kagoshima Prefecture in October 2016). These individuals were the same animals that had been used in previous color discrimination tests conducted by Takayama et al. (2018) and Nakamura et al. (2018) and were trained using a T-maze to follow a positive stimulus to receive a food reward. The experiment was conducted during daily management hours (5:00–20:00), and ad libitum intake of roughage (commercial oats hay, green ryegrass, and green field grass), water, and mineral salts were allowed. As a supplemental feed, commercial lucerne pellets (ingredients such as alfalfa meal and bran) were provided at different times (for example, immediately before and during the experiment). This feed was provided at a rate of 200–300 g per sika deer per day. In particular, the pre-experimental feeding of pellets (50–100 g) was intended to calm the sika deer agitation caused by their increased desire for feed.

Fig. 1.

A schematic diagram of the experimental enclosure. W: Waiting room, D: Door, : Partition, P: Panel, F: Feed trough, →: Route for deer, M: Monitoring room,: Digital video camera, : Infrared camera.

In the operant conditioning room, each deer was not exposed to any stimuli from the external environment that would affect the experiment, such as visual stimuli from sunlight or auditory stimuli derived from the movement of an observer. An LED lamp was used to illuminate the room, with the intensity of light at the center of the panel (P) being 150–200 lx. A digital video camera (DCR-SX41 or SR300; Sony, Tokyo, Japan) and four infrared cameras (SC-701R; OHM ELECTRIC, Tokyo, Japan) were installed in the operant conditioning room. The sika deer were observed and recorded exiting the waiting room (W), detecting and choosing the panel in front of a 3-m-long partition (1.1 m above the ground) extending from the center of a screen at a distance of 4 m in front of the waiting room door, and receiving food behind the screen (Fig. 2). The floor of the room comprised soil, on which square timber markers were placed at 1-m intervals from the panels to indicate distance and measurement points. The walls of the room were completely white, which would minimize the impact of light reflected off the wall on the panels. A Landolt ring, which is considered an international standard for the measurement of visual acuity in humans, was used to assess visual acuity of the sika deer based on changes in ring size. The size of the Landolt rings for each acuity value was also based on international standards, where the distance to the measurement point was 5 m and corrected to 3 m (Table 1). For the purpose of discrimination tests, a Landolt ring was used to provide a positive stimulus and an ordinary ring of equal size was used to provide a negative stimulus. The direction of the gap in the Landolt ring was always downward. A poster (750 mm × 500 mm) of each ring was attached to the plywood panels (800 mm × 600 mm × 3 mm), taking care to avoid wrinkles and the poster surface was covered with a 2-mm-thick sheet of transparent vinyl to prevent stains and damage.

Fig. 2.

Representative images of sika deer performing the discrimination test (C; Landolt ring, left; ordinary ring, right). The white circle in (D) indicates sika deer.

Table 1.

The size of Landolt rings corresponding to different visual acuity tests

The two panels (positive and negative) were suspended on both the right and left sides of the screen, the arrangement of which was determined randomly based on the throw of a dice. The trial commenced when the door of the waiting area was opened, and the test animal was allowed to freely choose either the left or right panels from the measurement point placed 3 m from the panels. A trial was terminated when the deer passed the measurement point. A trough filled with food was placed behind each side of the screen. The trough associated with the negative stimulus was covered with a wire mesh, which prevented access, although it still allowed the deer to see and smell the food. The trough associated with the positive stimulus was fitted with an open wire mesh allowing access to the reward. The deer only received a food reward [10 g/head (fresh matter basis) of lucerne pellets] after having initially selected the positive stimulus. After feeding, the deer returned to the waiting area. A new trial was initiated when the sika deer had been in the waiting area for approximately 1–2 min and the mean time for a trial was 1 min. Each session consisted of 20 trials, and the deer were subjected to one or two sessions per day. The criterion for successful discrimination was 15 or more correct choices in a total of 20 trials (75% correct choice rate, P < 0.05, chi-square test) over three consecutive sessions. If the test animals changed the panel to be selected after passing the measurement point, correct responses were not accepted. The tests were performed starting at a visual acuity of 0.02, with the value thereafter being sequentially increased to 0.04, 0.08, 0.16, and 0.24.

Prior to commencing the tests, preliminary training for the deer was conducted from June–July 2018. The first training was conducted using an ordinary ring with an overall diameter of 450 mm and width of 90 mm, respectively, for both positive and negative stimuli. The purpose of the training was to habituate the test animals to the apparatus and to eliminate factors that would have confounded the selection behavior of deer, such as a bias in the odor emitted from the feed trough on the left and right sides, dirt, or slight differences in the appearance of panels. For both individuals, preliminary training was completed in the 5th session, as at this stage they achieved approximately ten correct responses in 20 trial sessions, and the choice between left and right had become random. This confirmed that the subjects did not select positive stimuli based on cues other than the shape of the ring and that they did not show positional deflection. The purpose of the second training period was to enable the animals to associate the shape of the Landolt ring with a reward. Training was conducted using the Landolt ring (the positive stimulus) and ordinary ring (negative stimulus) at a visual acuity of 0.01. Immediately after the start of this training period, the proportions of correct responses for both individuals were around 50%. Although we had expected beforehand, it could be assumed that those were because the difference in the shape of the Landolt ring and ordinary ring had not yet been recognized by the test animals at that point. Therefore, the training was continued until we were able to determine that each individual had learned the relationship between shape and feed. The learning rate of discrimination differed between the two individuals, we completed the second training in the 44th and 6th sessions for the male and female, respectively, at which point they had made 15 or more correct choices in the 20 trials per session (75% correct choice rate, P < 0.05, chi-square test) over three consecutive sessions. The above training confirmed the “selection behavior of positive stimuli through the establishment of associative learning,″ and the sika deer were tested in the main test. The test animals were originally wild and very cautious, but we were able to control their behavior by carefully handling them in a manner that did not cause fear, such as avoiding unnecessary approach, contact, and noise, throughout the entire daily management and experiments.

Results

The proportion of correct responses for the male deer is shown in Fig. 3. In the 0.02 visual acuity test, the proportion of correct responses was 70% in the 1st session and 75% in the 2nd session, and subsequently, in the 3rd and 4th sessions it remained constant at a level of 75% for three consecutive sessions.

In the 0.04 visual acuity test, the proportion of correct responses was between 55% and 80% in the 1st to 5th sessions. In the 6th, 7th, and 8th sessions, the proportion of correct responses was 80%, 85%, and 75%, respectively, thus reaching the criterion value over three consecutive sessions. In the 0.08 visual acuity test, the proportion of correct responses was between 40% and 75% in the 1st to 6th sessions, and 75%, 85%, and 85% in the 7th, 8th, and 9th sessions, respectively, thereby reaching the criterion value over three consecutive sessions. In the 0.16 visual acuity test, the proportion of correct responses was between 50% and 80% from the 1st to 8th sessions, and 75%, 85%, and 85% in the 9th, 10th, and 11th sessions, respectively, thereby reaching the criterion value over three consecutive sessions. In the 0.24 visual acuity test, the proportion of correct responses was between 20% and 75% in the 1st to 20th sessions, and reached the criterion value in the 5th and 8th sessions; however, the deer failed to achieve consistent criterion values over three consecutive sessions. These findings accordingly indicated that the highest visual acuity of the male deer was 0.16.

The proportion of correct responses for the female sika deer is shown in Fig. 4. In the 0.02 visual acuity test, the proportions of correct responses in the 1st, 2nd, and 3rd sessions were 75%, 75%, and 55%, respectively. However, it increased to 80% in the 4th session and remained at 95% for the 5th and 6th sessions, thus reaching the criterion value over three consecutive sessions. In the 0.04 visual acuity test, the proportion of correct responses in the 1st to 9th sessions was between 50% and 90%, and in the 10th, 11th, and 12th sessions was 75%, 75%, and 85%, respectively, reaching the criterion value over three consecutive sessions. In the 0.08 visual acuity test, the proportion of correct responses was between 40% and 80% in the 1st to 16th sessions, 75% in the 17th session, and 80% in the 18th and 19th sessions, thereby reaching the criterion value over three consecutive sessions. In the 0.16 visual acuity test, the proportion of correct responses in the 1st was 70%, and reached 75%, 75%, and 80% in the 2nd, 3rd, and 4th sessions, respectively, thereby reaching the criterion value over three consecutive sessions. In the 0.24 visual acuity test, the proportion of correct responses was between 30% and 85% in the 1st to 20th sessions and reached the criterion value in the 2nd and 18th sessions, although failed to reach the criterion value over three consecutive sessions. Thus, similar to the male deer, these observations indicated that the highest visual acuity of the female deer was 0.16.

Fig. 3.

Proportion of correct responses by a male sika deer in discrimination tests using Landolt (positive stimulus) and ordinary (negative stimulus) rings. The values in tortoise shell brackets indicate visual acuity.

Discussion

One of the measures of humans to understand the shape of objects is the minimum separable, that is, the threshold at which two points or two lines can be distinguished and perceived, and this ability is called visual acuity (Kobayashi et al. 2022). In the usual visual acuity measurement using a Landolt ring, a person can read a Landolt ring with an outer diameter and width of 7.5 and 1.5 mm at a distance of 5 m, respectively (Kobayashi et al. 2022). This corresponds to a visual acuity of 1.0. For example, when five Landolt rings are arranged in the same row on the visual acuity chart, the criterion is that the direction of at least three of the rings must be known (Kobayashi et al. 2022). In contrast, in cattle (Manda et al. 1993), sheep (Ovis aries) (Tanaka et al. 1995), and pigs (Tanaka et al. 1998), visual acuity was measured on the basis of these animals being able to discriminate between a Landolt ring with a uniform gap position and a circle of the same size as the visual target. The criterion was determined by the number of correct responses per session, which was 16/20 trials (P < 0.01) for cattle (Manda et al. 1993), and 21/30 trials (P < 0.05) for both sheep (Tanaka et al. 1995) and pigs (Tanaka et al. 1998), and the strict criterion of reaching the standard value in two to three consecutive sessions, improving the accuracy of the experiment. However, to the best of our knowledge, no studies have been conducted on the visual acuity of sika deer. In this study, we established that these deer can learn to discriminate between positive and negative visual stimuli and that their visual acuity can be effectively measured using Landolt rings as visual targets in an operant learning experiment with setting the same strict criterion. It is known that there are individual differences in learning rate (Sugnaseelan et al. 2013), and it was reported that it took 20–280 trials for cattle (Manda et al. 1993), 240–360 trials for sheep (Tanaka et al. 1995), and 240–2220 trials for pigs (Tanaka et al. 1998) to establish association learning. It is assumed that similar individual differences were also reflected in the number of trials through the learning training for sika deer in this study, approximately 160–880 trials (8–44 sessions), but both individuals were able to complete the training, and the main test was subsequently proceeded without interruption. We found that both the male and female sika deer we assessed have a visual acuity of 0.16. In behavioral tests using operant learning experiments with square-wave gratings, the spatial resolution of red deer (Cervus elaphus hippelaphus) was found to be 2.65 cycles/degree (n = 1) with 500 lx (Backhaus 1959, as cited by Sugnaseelan et al. 2013), whereas that in white-tailed deer (Odocoileus virginianus) was between 4 and 6 cycles/degree (n = 3) with visual target of mean luminance 61.33 cd/ m² (Watson et al. 2022). Based on a conversion of these values, we estimate that the visual acuity of red deer would be ∼0.09 and that of white-tailed deer would be 0.13–0.2. The illuminance of the visual target in the previous studies (Backhaus 1959, as cited by Sugnaseelan et al. 2013; Manda et al. 1993; Tanaka et al. 1995, 1998) was controlled by artificial lighting installed in the room or by lighting from screen of visual target itself (Watson et al. 2022). Although 200 lx is the standard illuminance of the visual target in human visual acuity testing, the illumination of the room should ideally not exceed 200 lx (Tokoro 1998). Additionally, another method is to adjust the illuminance of the visual target to approximately 500 to 1000 lx, and the illumination of the room should not exceed this level (Kobayashi et al. 2022). Therefore, it is apparent that the illuminance in the previous and the current studies has been within the standard range. Both gratings and Landolt rings are commonly used optotypes in experiments of visual acuity in animals and young children (Sugnaseelan et al. 2013), and the visual acuity of 0.16 obtained in the present study is higher than that estimated for red deer and within the range of estimates for white-tailed deer. However, given the limited sample sizes of the animals assessed in these studies, including present study, further research would be necessary to gain a more accurate picture of the differences in visual acuity among individuals within sika deer and among different cervid species.

Fig. 4.

Proportion of correct responses by a female sika deer in discrimination tests using Landolt (positive stimulus) and ordinary (negative stimulus) rings. The values in tortoise shell brackets indicate visual acuity.

Compared with predatory animals, such as cats (Felis catus), herbivorous ungulates such as cattle and sheep are known to have narrower binocular vision and wider monocular vision (Houpt and Wolski 1982), and are generally considered to have poor visual acuity. In cattle and sheep, visual acuity values of 0.04–0.08 with approximately 825 lx (n = 5) (Manda et al. 1993) and 0.085–0.19 (n = 3) with approximately 500 lx (Tanaka et al. 1995), respectively, have been obtained using Landolt rings, with even lower acuity values of 0.017–0.07 (n = 6) being obtained for pigs with 500–550 lx (Tanaka et al. 1998), whose ancestors are wild boars known to be active even nocturnally. It can be speculated that differences in visual acuity among animals may be associated with differences in the topography of the landscapes within which they have evolved (Sugnaseelan et al. 2013). Hearing is more important in forests with poor visibility, while vision is more important in grasslands with good visibility (Geist 1987). Vision is the most important sense for horses (Equus caballus) (Takimoto et al. 2011). In behavioral tests using operant learning experiments with square-wave gratings, the spatial resolution of horses was found to be 18.4–23.3 cycles/degree with approximately 30 cd/m² (n = 3) (Timney and Keil 1992), and the visual acuity of them would be 0.61–0.78. The feeding and behavioral characteristics of sika deer tend to indicate that these animals have become adapted to undulating forest environments (Takatsuki 2006). Although deer rely primarily on hearing and olfaction to monitor changes in their environment, their vision is an essential complement to confirm what the other senses detect and to move accordingly (VerCauteren and Pipas 2003). The fact that the visual acuity of sika deer is higher than that of cattle (Manda et al. 1993) and pigs (Tanaka et al. 1998) may indicate that identification of objects by vision is more important to sika deer than to these species. Whereas, in Japan, remains of sika deer have been frequently found in archaeological artifacts from the Jomon Period (Nishimoto 1995), providing evidence that points to this species not being restricted to inhabiting forests but also inhabiting open plains for prolonged periods (Takatsuki 2006). Sheep evolved in open undulating montane habitats that required acute vision for food selection and predator detection in both the vertical and horizontal planes (Sugnaseelan et al. 2013), and the visual acuity of the animal (Tanaka et al. 1995) is comparable to that obtained for sika deer. The visual acuity of sika deer may be one of the reasons why this species has survived and plastically adapted to environments with different visibility conditions and topography.

In their investigation of the visual acuity of cattle, Manda et al. (1993) revealed the generally poor eyesight of these animals, whereas in earlier studies, Manda et al. (1989a) demonstrated the color discriminatory ability of cattle and Manda et al. (1989b) identified differences in their behavioral responses to the color of electric wire. These latter findings indicate that cattle are unable to readily detect the thin wire of electric fences, and that 1.0-cm-thick red ribbon wire, which could be detected at distances greater than 4 m, would contribute to preventing escape and enhance overall grazing management (Manda et al. 1989b).

With respect to the vision of sika deer, it has been suggested that these deer can distinguish colors under both light and dark conditions (Takayama et al. 2018; Nakamura et al. 2018, 2021), and that their visual acuity is two- to four-fold higher than that of cattle (Manda et al. 1993). The specialized light control functions of deer eyes enable these animals to maintain high visual acuity during bouts of diurnal and nocturnal activity (Müller-Schwarze 1994), and thus, when necessary, enables them to shift their activity patterns to nighttime to avoid human activity (Tsukada 2012). These findings indicate that regardless of the time of day, sika deer employ their color vision and visual acuity to register information such as object colors, gaps between objects, and shapes in the external environment. In cases in which these deer pass through fences, it is believed that they can detect even small gaps in protective fences and use these as entry points, indicating that sufficient repair of the bases of such fences and other necessary repairs should be thoroughly conducted during daily maintenance. Using a visual acuity of 0.16, it is calculated that a gap of 2 mm in the Landolt ring can be distinguished at a distance of 1.1 m. In addition, it has been reported that when sika deer try to pass through electric fences, they do not run from a distance, but rather approach with their head in a protruding posture until the distance between their front legs and the fence is within one meter (Nakamura et al. 2022a, 2022b). Therefore, considering electric fences, unlike cattle, it is presumed that sika deer can detect the color, shape, and vertical arrangement of 2-mm-width wires extending horizontally long. Accordingly, it is assumed that effective invasion prevention could be achieved by installing the wires at appropriate heights and conducting daily management, such as confirming the energization and mowing the grass along fence boundaries. In contrast, a method of dealing with situation in which sika deer have learned to pass through electric fences is to control their behavior by shortening the distance between wires around the height where they frequently pass, taking advantage of the fact that sika deer can visually recognize the size of gaps. Alternatively, it may be possible to reduce the visibility of electric wires, i.e., to use inconspicuous color and thin wires that sika deer can only detect at close range, thereby inciting fear, inducing more contact with their noses, and ensuring that electrical stimulation is provided. The important thing would be to combine information on the visual perception of sika deer to improve fences and develop new countermeasures according to the characteristics of them.

In conclusion, the results of our operant learning experiments using Landolt rings indicate that sika deer have a visual acuity of up to 0.16, which is comparable to that of white-tailed deer and sheep. With a view toward reducing human–wildlife conflicts and economic losses associated with the invasion of agricultural land by sika deer, in addition to visual stimuli, future studies should also consider other sensory cues (e.g., auditory and olfactory) and behavioral traits (e.g., memory and boldness) related to the interactions between sika deer and materials of invasion prevention. In situ behavioral experiments could also be beneficial in revealing the behavior and ecology of sika deer in modified landscapes, and in the development of appropriate prevention systems.