Observations of predation attempts on avian nest boxes by Japanese martens (Martes melampus)
Craig A. Barnett1, Norimasa Sugita1,2 and Toshitaka N. Suzuki1,3,*1 Department of Life Science, Rikkyo University, 3-34-1 Nishi-Ikebukuro, Toshima-ku, Tokyo 171-8501, Japan2 National Museum of Nature and Science, Tsukuba 305-0005, Japan3 Department of Evolutionary Studies of Biosystems, The Graduate University for Advanced Studies, Hayama, Miura-gun, Kanagawa 240-0193, Japan
Predation is an important biological factor, which influ-ences animal populations (see Newton 1998 for a review). Observations of natural predatory events are imperative for understanding the effects of this selective pressure on the survival and reproductive success of animal popula-tions (Clutton-Brock 1988). Yet, despite the pervasive effects of predation, observations of natural predatory events are rare in the study of animal ecology.
In many environments, avian nests may face different risks posed by multiple types of predators (e.g., birds, mammals, and reptiles). In Japan, small passerines may have their nests depredated by a wide variety of predators such as Jungle crows (Corvis macrorhynchos), Japanese martens (Martes melampus), and Japanese rat snakes (Elaphe climacophora) (Suzuki and Ueda 2013). Each of these species presents different challenges to both parents and offspring in avoiding predation, and species may evolve predator-type specific behaviors to deal with these different predators (Suzuki 2011, 2012). However, single predator species (such as martens) can have a significant effect on the nesting success of small passer-ines (Yamaguchi et al. 2005).
Japanese martens are opportunistic omnivorous forag-ers and fecal analyses reveal that they eat mainly fruits, plant material, insects, and small mammals (Tatara and Doi 1994; Arai et al. 2003). While Japanese martens are suspected nest predators of small birds (Yamaguchi et al. 2005; Yamaguchi and Higuchi 2005), there is no direct observation of Japanese martens destroying the nests of small passerines in order to eat their contents. However, this may be because Japanese martens are very secretive and hard to observe under natural conditions.
The hunting behavior of Japanese martens in their natural environments is poorly understood. Adult mar-tens maintain exclusive territories that range in area from
0.6 km2 to 3 km2 with little overlap between territories and with territory size varying depending on food avail-ability and sex (Kawauchi et al. 2003). There are also few data describing how Japanese martens behave throughout the day and throughout the year. Musteline predators are opportunistic hunters and so can change their behavior depending on changes in food availability throughout the year (Zielinski 2000). For example, a closely related species to Japanese martens, the American marten (Martes americana), is known to vary the times of their hunting activity between seasons with animals hunting diurnally in the summer and nocturnally during the winter (Zielinski et al. 1983). It is assumed that Japanese martens (like most other mustelids) are primarily noctur-nal although their activity can vary in relation to food availability and other environmental factors (Zielinski 2000). There have been a small number of observations of Japanese martens being diurnally active. For example, Japanese martens have been seen mating in the early morning and evening, which suggests that they may be active during these times (Tatara 1994). However, there is little direct evidence of Japanese martens hunting during daylight hours.
Here, we describe the results of observations that were made at 24 Japanese great tits (Parus major minor) nests and 1 coal tit (Periparus ater) nest that were monitored with infrared cameras. These observations confirmed that Japanese martens are significant predators of Japanese great tits nesting in our study areas and that martens have a predominantly crepuscular pattern of visitation. Our observations also show how martens depredate the contents of artificial nest boxes at our study site, which is the first time this behavior has been filmed or photographed.
*To whom correspondence should be addressed. E-mail: [email protected]
These observations were made in mixed woods at Karuizawa, in Nagano Prefecture, Japan (36°21–22'N, 138°35–36'E) between 6 June and 23 June, 2011 and between 22 May and 20 June, 2012. The woods are secondary forest and are composed mainly of Japanese larches (Larix kaempferi), giant dogwoods (Cornus controversa), Japanese elms (Ulmus davidiana), and Japanese oaks (Quercus crispula). Great tits and coal tits are a cavity nesting species that readily nest in artificial nest boxes. We placed a total of 60 nest boxes throughout the forest in 2011 and 83 nest boxes in 2012. The nest boxes were placed no less than 30 m from one another and titmice (mostly great tits) regularly use these sites in which they build nests. We numbered nest boxes by writing a unique number on their front. Nest box height was about 1.8 m from the ground. Although there are many species of nest predators at Karuizawa (e.g.,
Japanese rat snakes and jungle crows, Suzuki and Ueda 2013), Japanese martens are thought to be among the most common predators of titmice nests. In order to study avian biology at Karuizawa we have had to use various innovations to reduce the impact of martens on nesting birds (e.g., Yamaguchi et al. 2005). We moni-tored predation events on a total of 25 active nests by placing Moultrie D55IR infrared digital cameras (Moultrie Feeders, Alabaster, Alabama, USA) between 3–5 m in front of the nests for a total of 197 days (Table 1). These cameras are triggered when they detect infrared heat sources, such as those radiated by mammals in the camera’s field of view. We programed the camera to take a photo every 30 sec when the camera detected a heat source and to record either 10 sec (2011) or 30 sec (2012) of video. We watched all videos and shutter re-leases to determine whether we could identify individuals based on their behavior, the time of visit, the proximity to other visits, and pelage markings of the martens.
Table 1. Monitoring of nest boxes used by great and coal tits
Species Year Date erected Nest number Duration (Days) Number of visits (visits per day) Marten predation*
Barnett et al., Bird nest predation by Japanese martens 271
Results
During the study periods, 32% (8/25) of titmice nest boxes that we monitored were visited by Japanese mar-tens. The martens made a total of 15 visits to these 8 nests, which provided an average visitation rate of 0.08 ± 0.03 (± SE) visits/nest/day. However, 5 of the visits for nest 7 in 2011 were made between 23:41 hr (Japan Standard Time [JST]) on 14 June and 03:58 hr (JST) on 15 June, which suggests that one individual made these visits. This nest was visited again at 07:39 hr (JST) on 16 June. The overall pattern of visitation was predomi-nantly during early morning and to a lesser extent in the evening (Fig. 1). Moreover, the majority of visits occurred diurnally with only 5 out of 15 visits (33%) occurring in darkness.
In most cases, we were unable to identify individual martens because the low quality of the night footage and the animals being at the wrong angle for us to make an identification. However, we determined the same indi-vidual might have been responsible for the visits we recorded at the two nests in 2011. This assessment was based on the proximity of the nests to one another and the pelage patterns on the front and back of the marten’s neck. A marten visited nest box 7, six times between 23:00 hr (JST) on 14 June and 04:00 hr JST on the 15 June. Thirteen-minutes after the last visit at nest box 7, the marten was photographed and filmed at nest box 3. Nest box 3 is approximately 300 m from nest box 7, which indicates that martens can move through their habitat very quickly. The marten was photographed for the final time at 07:39 hr JST on 16 June. In 2012, mar-
tens visited nests over wide areas, and although we could not definitively identify individuals, the spatial distribu-tion of visits would indicate that the visits in 2012 were made by up to three different individual martens.
The primary method that martens used to attack nests was to climb onto the top of the nest box and reach down and use their forelimbs to grasp and pull the nest material from its entrance (http://zoo2.zool.kyoto-u.ac.jp/ethol/mov/13/1302/momo130227jm01.AVI, Fig. 2a). How-ever, we once observed a marten attached itself to the front of the nest box with its hind legs in order to reach into the nest box and pull material from it (Fig. 2b). Any eggs or nestlings in the nest were pulled out with the material, which the marten then chewed and ate (Fig. 3).
Fig. 1. The number of marten visits in relation to time of day and light levels (from movie data). The black bars indicate a marten visit in darkness and the white bars indicate visits during daylight hours. The martens made the majority of nest visits early in the morning and to a lesser extent in the evening.
Fig. 2. Different methods used by martens to gain access to nest boxes so they could then pull nest material from the nest. Martens either balanced themselves off the top of the nest box and reached into the nest box from above (a) or held onto the front of the nest box with their hind legs from below the nest entrance and reached into the nest box using their front legs (b).
272 Mammal Study 38 (2013)
The marten left the remaining nest material scattered on the ground or on top of the nest box and it sometimes contained nestling remains (T. N. Suzuki, personal obser-vation).
Discussion
We have provided the first observations of Japanese martens hunting diurnally and attacking the nests of small passerines. While previous studies have suggested that Japanese martens are significant nest predators of small passerines (Yamaguchi et al. 2005; Yamaguchi and Higuchi 2005), direct observation of their hunting tech-nique has proved elusive. Although Japanese martens are normally considered nocturnally active, mustelids are omnivorous and opportunistic hunters (Zielinski et al. 1983). Therefore, martens might have been changing their behavior during the spring to take advantage of the nestling begging and parental feeding visits to their nests. If martens were active throughout the day for large parts of the year, one would assume there would be more records of marten activity at these times.
Although martens are omnivorous and opportunistic predators, these data show the potential for martens to be significant predators of passerine nests. Martens visited 32% of nests monitored in this study and these nests would have stood a high chance being depredated had it not been for the modifications that were made to the nest boxes. In 2012, we made the overhang of the next box lids longer in order to reduce the ability of martens to reach into the nest box and grab nest material. Subse-quently, only 2 out of the 7 nest boxes that were visited by
martens failed as a result of marten predation in 2012. Therefore, extending the edge of the nest box lid well past the edge of the nest box in addition to the modifications suggested by Yamaguchi et al. (2005) may be effective at reducing predation of titmouse nests.
All the nest visits made by martens occurred later in the breeding cycle, when nests contained nestlings. This suggests that martens may have been using smell and auditory cues to find nests. The observations of the visi-tations of the marten in 2011 indicate that individual martens may remember the location of nest boxes and may regularly visit them. However, it is unknown whether martens use specific cues, rely on search images, or systematically investigate all nest boxes they encoun-ter. It might be the case that martens use many techniques to find active nests. For example, martens may find nests using the parent’s alarm calling or provisioning flights (e.g., Martin et al. 2000), nestling vocalizations (e.g., Leech and Leonard 1997), or the nest boxes themselves as search images. However, nest boxes tend to have similar rates of predation compared with natural nests (Møller 1989; Robertson and Rendell 1990; Miller 2002). It would be valuable to compare the rates of marten visi-tation for active nests to empty nest boxes to determine marten hunting strategies.
Of the 8 nests that were visited by martens, 6 were visited during daylight hours. The majority of these visits were in the morning after sunrise, but before 08:00 hr and there were a small number of visits in the evening. Although Japanese martens are thought to be mainly nocturnal, they may adopt a more crepuscular activity pattern during the nestling period of avian reproduction. Mustelids are known to be opportunistic hunters and often have plastic activity patterns allowing them to take advantage of changes in seasonal food availability (as may happen during avian reproduction) (Zielinski 2000). Moreover, early in the morning, nestlings may have low energetic reserves having fasted the entire night. There-fore, nestling begging may be particularly vociferous at this time and parents may make many feeding visits to their nest to meet the energetic demands of nestlings (Best 1977; Nolan 1978; Pinkowski 1978). This increased begging and feeding activity may make nests more con-spicuous to martens at this time (e.g., Martin et al. 2000; Pärt and Doligez 2003; but see Halupka and Greeney 2009).
Martens maintain almost exclusive territories, so it is likely that multiple visits to individual nest boxes (e.g., nest boxes 7, 69, and 80), were made by the same indi-
Barnett et al., Bird nest predation by Japanese martens 273
vidual martens. However, territories of American mar-tens can overlap by approximately 10% (Buskirk and Ruggiero 1994) and so it is possible that more than one individual made visits to the same nest box. Although the visits at both nest boxes in 2011 were likely by the same individual, it is more difficult to estimate the number of martens that visited nest boxes in 2012. However, given the spatial range over which the visits occurred (several kilometers) and the territorial behavior of martens, it is likely that at least 3 individual martens visited different nest boxes in 2012.
Our observations also showed that martens might have different tactics for pulling the contents from nests. In most cases, the martens suspended themselves from the top of the nest box and reached down into the nest box with their forelimbs (Fig. 2a). However, on one occasion, a marten attached itself to the front of the nest box below the entrance and reached into it with its forelimbs (Fig. 2b). It is tantalizing to think that this might represent a case of problem solving as the day before the photograph in Fig. 2b was taken, an individual (probably the same as in Fig. 2b) had visited the nest box and unsuccessfully tried to pull material from the nest box by standing on the top of the nest box (see video link). If this is the case, this indicates that martens are intelligent and persistent preda-tors and may be good problem-solvers. However, more research is required on marked individuals before we can be certain such observations represent problem solving in Japanese martens.
In conclusion, we have provided evidence of the cre-puscular hunting pattern by Japanese martens during the spring and the methods by which they may use to attack nests. These observations confirm previous concerns that martens may be significant predators of nests in some bird populations (Yamaguchi et al. 2005; Yamaguchi and Higuchi 2005). However, it was not the purpose of this study to document the effects of marten predation on passerines. Moreover, our data show that martens hunt during the day during the spring which is an uncommon time for activity in this species. While martens are major predators of nests, great tits have other predators (e.g., crows and snakes; Suzuki and Ueda 2013), which can seriously impact small bird populations (Yamaguchi et al. 2005). Therefore, more research is required to uncover the daily and seasonal activity patterns of Japanese martens in concert with other predators and to understand the combined effects of all predators on small bird populations.
Acknowledgments: This research was supported by a Grant-in-Aid for the Japan Society for the Promotion of Science (JSPS) Fellows (grant no: 23.01701) to CAB. We thank two anonymous referees for their comments, which helped to improve this manuscript.
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