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Temporal differences in breeding site use between tits and mice

ABSTRACT

Describing the interactions among cavity breeders is key to understanding their breeding ecology. In this study the temporal difference in cavity use between the great tit, Parus major (Linnaeus, 1758) and the small Japanese field mice, Apodemus argenteus (Temminck, 1845) is investigated, as a first step for clarifying the interaction between bird and mammal cavity breeders. Forty-seven nest boxes were installed on tree trunks in two urban forests of Hokkaido Island, Japan, and the breeding nests of tits and mice were found in 34 and 11 boxes, respectively. The tits used the nest boxes throughout the breeding season, from May to July. In contrast, mice breeding nests were found in the last half of the breeding season, from July to October. Our results showed that field mice rarely used boxes during the tits’ breeding season. This study provides important information, such as temporal differences in breeding site use between tits and mice.

KEY WORDS:
Bird-mammal interaction; breeding ecology; competition; reproduction strategy; tree cavities

Tree cavities are used as breeding and nesting sites by numerous wildlife species (Martin and Eadie 1999Martin K, Eadie JM (1999) Nest webs: A community-wide approach to the management and conservation of cavity-nesting forest birds. Forest Ecology and Management 115: 243-257. https://doi.org/10.1016/S0378-1127(98)00403-4
https://doi.org/10.1016/S0378-1127(98)00...
, Martin et al. 2004Martin K, Aitken KEH, Wiebe KL (2004) Nest sites and nest webs for cavity-nesting communities in interior British Columbia, Canada: Nest characteristics and niche partitioning. Condor 106: 5-19. https://doi.org/10.1650/7482
https://doi.org/10.1650/7482...
). There are several types of interactions among cavity users. Understanding these interactions is crucial for accurately understanding the ecology of cavity breeders (e.g., Minot and Perrins 1986Minot EO, Perrins CM (1986) Interspecific interference competition - Nest-sites for Blue and Great tits. Journal of Animal Ecology 55: 331-350. https://doi.org/10.2307/4712
https://doi.org/10.2307/4712...
, Newton 1994Newton I (1994) The role of nest-sites in limiting the numbers of hole-nesting birds: a review. Biological Conservation 70: 265-276. https://doi.org/10.1016/0006-3207(94)90172-4
https://doi.org/10.1016/0006-3207(94)901...
), since cavity users often segregate spatially and/or temporally in the use of cavities, thus avoiding competition. For example, the small Japanese field mouse, Apodemus argenteus (Temminck, 1845), nests in cavities near the ground, to avoid competition with the Siberian flying squirrel, Pteromys volans (Suzuki and Yanagawa 2012Suzuki K, Yanagawa H (2012) Different nest site selection of two sympatric arboreal rodent species, Siberian flying squirrel and small Japanese field mouse, in Hokkaido, Japan. Mammal Study 37: 243-247. https://doi.org/10.3106/041.037.0308
https://doi.org/10.3106/041.037.0308...
, Suzuki et al. 2014Suzuki K, Yamane Y, Yanagawa H (2014) Nest site use by the small Japanese field mouse: possibility of nest height change in the presence of the Siberian flying squirrel. Mammalian Science 54: 243-249.). Also, the pied flycatcher Ficedula hypoleuca (Pallas, 1764) and the great tit Parus major (Linnaeus, 1758) have different breading seasons and that increases the breeding success of the flycatcher (Slagsvold 1978Slagsvold T (1978) Competition between the great tit Parus major and the pied flycatcher Ficedula hypoleuca: an experiment. Ornis Scandinavia 9: 46-50. https://doi.org/10.2307/3676138
https://doi.org/10.2307/3676138...
).

Intra-class interactions, such as mammal-mammal (Shafique et al. 2009Shafique CM, Barkati S, Oshida T, Ando M (2009) Comparison of nest trees of two sympatric flying squirrel species in northern Pakistan. Mammalian Biology 74: 240-244. https://doi.org/10.1016/j.mambio.2009.01.005
https://doi.org/10.1016/j.mambio.2009.01...
, Nakamura-Kojo et al. 2016Nakamura-Kojo Y, Kojo N, Tamate HB (2016) Spatial differences in arboreal activity of two rodents, the Japanese dormouse (Glirulus japonicus) and the small Japanese field mouse (Apodemus argenteus). Annals Zoologici Fenici 53: 81-92. https://doi.org/10.5735/086.053.0207
https://doi.org/10.5735/086.053.0207...
) or bird-bird (Minot and Perrins 1986Minot EO, Perrins CM (1986) Interspecific interference competition - Nest-sites for Blue and Great tits. Journal of Animal Ecology 55: 331-350. https://doi.org/10.2307/4712
https://doi.org/10.2307/4712...
, Newton 1994Newton I (1994) The role of nest-sites in limiting the numbers of hole-nesting birds: a review. Biological Conservation 70: 265-276. https://doi.org/10.1016/0006-3207(94)90172-4
https://doi.org/10.1016/0006-3207(94)901...
) have been more thoroughly investigated. Inter-class -bird-mammal interactions, in contrast, are likely to go unrecognised and have been systematically ignored by scientists, despite the fact that they are important to understand cavity-breeding ecology (Czeszczewik et al. 2008Czeszczewik D, Walankiewicz W, Stanska M (2008) Small mammals in nests of cavity-nesting birds: why should ornithologists study rodents? Canadian Journal of Zoology 86: 286-293. https://doi.org/10.1139/Z07-139
https://doi.org/10.1139/Z07-139...
). As a first step to study these interactions, it is important to try to ascertain the different uses of breeding cavities (Suzuki and Yanagawa 2012Suzuki K, Yanagawa H (2012) Different nest site selection of two sympatric arboreal rodent species, Siberian flying squirrel and small Japanese field mouse, in Hokkaido, Japan. Mammal Study 37: 243-247. https://doi.org/10.3106/041.037.0308
https://doi.org/10.3106/041.037.0308...
) and to clarify the interactions among cavity users (Suzuki et al. 2014Suzuki K, Yamane Y, Yanagawa H (2014) Nest site use by the small Japanese field mouse: possibility of nest height change in the presence of the Siberian flying squirrel. Mammalian Science 54: 243-249.). In this contribution, we surveyed the breeding sites of great tits and small Japanese field mice, some of the most abundant, similarly sized (10 to 20 g) cavity breeders in Japanese forests, to provide information on the temporal and spatial differences in how they use breeding cavities.

To survey the breeding site uses by the two species, we installed 47 handmade, wooden nest boxes within a total of approximately 9.8 ha bordering two urban forests (42°51’ to 42°53’N, 143°09’ to 143°11’E) in the Tokachi area of eastern Hokkaido, Japan, on 8 and 9 June 2011. Details on the environments of survey forests are shown in Suzuki et al. (2016Suzuki K, Yamane Y, Yanagawa H (2016) Invasive cutleaf coneflower seeds cached in nest boxes: Possibility of dispersal by a native rodent. Plant Species Biology 31: 300-303. https://doi.org/10.1111/1442-1984.12115
https://doi.org/10.1111/1442-1984.12115...
). On Hokkaido Island, the breeding seasons of the two species largely overlap. The main breeding season of great tits is from May to July, and they rarely breed in August (Yuta and Koizumi 2012Yuta T, Koizumi I (2012) Long breeding season and high frequency of multiple brooding in great tits in Northern Japan. Ardea 100: 197-201. https://doi.org/10.5253/078.100.0211
https://doi.org/10.5253/078.100.0211...
). In mice, reproductively active females are found from April to September (Fujimaki 1969Fujimaki Y (1969) Reproductive activity in Apodemus argenteus Temminck. Journal of Mammalogical Society of Japan 4: 74-80.).

Other cavity nesters in this area are the Eurasian nuthatch, Sitta europaea (Linnaeus, 1758), and the Siberian flying squirrel, Pteromys volans (Linnaeus, 1758) (Suzuki et al. 2016Suzuki K, Yamane Y, Yanagawa H (2016) Invasive cutleaf coneflower seeds cached in nest boxes: Possibility of dispersal by a native rodent. Plant Species Biology 31: 300-303. https://doi.org/10.1111/1442-1984.12115
https://doi.org/10.1111/1442-1984.12115...
). We are confident that, during the observation period, the nest boxes were not used by either species. The nests of the nuthatch are easily identifiable by the size of their entrance, which is reduced by smeared pellets of dirt, and flying squirrels are too big for the, small circular entrance of the nest box (diameter 2.5 cm) (Suzuki et al. 2014Suzuki K, Yamane Y, Yanagawa H (2014) Nest site use by the small Japanese field mouse: possibility of nest height change in the presence of the Siberian flying squirrel. Mammalian Science 54: 243-249.). The boxes were uniform in size (24 cm high × 8 cm wide × 18 cm deep), walls 2.5 cm thick, and were installed at a distance of more than 20 m apart in the forests. This distance was adopted because the distance among the naturally occurring breeding nests of the mice is approximately 20 m (Setoguchi 1981Setoguchi M (1981) Utilization of holes and home ranges in the Japanese long-tailed mice (Apodemus argenteus). Japanese Journal of Ecology 31: 385-394.). Nest boxes were installed from 0.7 m to 2.8 m from the ground. By doing this, we aimed to ascertain the spatial differences in breeding sites, since cavity height plays an important role in predator avoidance, and cavity-nesting animals often use different heights to avoid competition (Suzuki and Yanagawa 2012Suzuki K, Yanagawa H (2012) Different nest site selection of two sympatric arboreal rodent species, Siberian flying squirrel and small Japanese field mouse, in Hokkaido, Japan. Mammal Study 37: 243-247. https://doi.org/10.3106/041.037.0308
https://doi.org/10.3106/041.037.0308...
, Suzuki et al. 2014Suzuki K, Yamane Y, Yanagawa H (2014) Nest site use by the small Japanese field mouse: possibility of nest height change in the presence of the Siberian flying squirrel. Mammalian Science 54: 243-249.).

We checked the boxes monthly from July to November 2011. From December 2011 to February 2012, we were unable to check them due to heavy snow cover. We checked the boxes again in early March 2012, at which time the nest materials of the previous year were removed from all nest boxes to prevent old nest materials in the nest boxes from being used in the second year. At that time, neither species had started breeding in any of the nest boxes. From May to October 2012, the boxes were checked twice a month. When adult great tits, eggs, and/or chicks were found in a nest box, we recorded the nest as a tits breeding site. When small Japanese field mice and/or neonates were found in the boxes, we recorded the nest as a mice breeding site.

We treated the first year as a habituation period, since nest utilisation by vertebrates usually starts many months after installation of the boxes (Ando 2005Ando M (2005) Improvement of nest box investigation techniques for study of arboreal rodents. Mammalian Science 45: 165-176.). Therefore, we used data from the second survey year, from May to October 2012, for the two analyses described below. To clarify temporal differences in cavity use between great tits and small Japanese field mice, we counted the number of nest boxes used for breeding per nest box check and evaluated the correlation of nest box uses between tits and mice using Spearman’s rank correlation. In addition, we constructed a logistic regression model to determine the spatial difference between the breeding sites of tits and mice. In this model, we treated the presence of tits or mice as a categorical dependent variable. Nest box height was treated as a continuous independent variable. The effect of the independent variable was evaluated using a χ2 test. These analyses were run in the statistical software R ver. 3.2.4 (R Core Team 2016R Core Team (2016) R: A language and environment for statistical computing. Vienna, R Foundation for Statistical Computing, https://www.R-project.org
https://www.R-project.org...
).

From May to October 2012, tits and mice bred in 34 and 11 nest boxes, respectively. While it appears that the proportion of boxes used by mice was relatively low, it did not differ much from results obtained by previous surveys using nest boxes (14/87 nest boxes, from July to October 2010) and natural cavities (21/136 natural cavities, from May to October 2009 and from May to October 2010) (Suzuki and Yanagawa 2012Suzuki K, Yanagawa H (2012) Different nest site selection of two sympatric arboreal rodent species, Siberian flying squirrel and small Japanese field mouse, in Hokkaido, Japan. Mammal Study 37: 243-247. https://doi.org/10.3106/041.037.0308
https://doi.org/10.3106/041.037.0308...
) in the area. The great tit used the nest boxes from early May to mid-July, and there was a mono-modal peak of use around mid-May to early June (Fig. 1). After this, the number of tits breeding in the boxes rapidly decreased, and no breeding was recorded in early August. In contrast, small Japanese field mice used the boxes from early July, when the breeding of the tits had almost ceased (Fig. 1). Bimodal peaks of mice breeding were recorded around early August and early October. The mean heights of the boxes used by the great tits and mice were 1.47 ± 0.58 (SD) m and 1.45 ± 0.62 m, respectively.

Figure 1
Number of nest boxes used by Parus major and Apodemus argenteus in 2012. On the x-axis, E indicates “Early” and M indicates “Middle”.

There was little overlap between the breeding periods of tits and mice (Fig. 1, z = -2.59, p = 0.01) in the nest boxes. In other words, a negative correlation was shown in nest box use between tits and mice. The height of the nest boxes used by the two species was quite similar (Fig. 2, χ2 = 0.02, p = 0.88). Although the tits used the nest boxes throughout their breeding season (Fig. 1), mainly from May to July (Yuta and Koizumi 2012Yuta T, Koizumi I (2012) Long breeding season and high frequency of multiple brooding in great tits in Northern Japan. Ardea 100: 197-201. https://doi.org/10.5253/078.100.0211
https://doi.org/10.5253/078.100.0211...
), the mice only used the boxes on the last half (Fig. 1) of their main breeding season, April to September (Fujimaki 1969Fujimaki Y (1969) Reproductive activity in Apodemus argenteus Temminck. Journal of Mammalogical Society of Japan 4: 74-80.). This is in contrast to a report that mice use nest boxes throughout their breeding season on the Kyushu Island (Sakata et al. 2009Sakata T, Nakazono T, Kaoka H, Tanoue H, Amano M (2009) Confirmation of Japanese flying squirrel (Pteromys momonga) with nest boxes in Gokanosho and Naidaijin, Kumamoto Prefecture, Japan. Bulletin of Kumamoto Wildlife Society 5: 11-20., 2010Sakata T, Yasuda M, Nagamine S (2010) Confirmation of Japanese flying squirrel (Pteromys momonga) and Japanese dormouse (Glirulus japonicas) in Ookawa, Minamata city, Kumamoto prefecture, Japan. Bulletin of Kumamoto Wildlife Society 6: 23-28.), where there was no overlap between the breeding seasons of mice (Yoshida 1972Yoshida H (1972) Small mammals of Mt. Kiyomizu, Fukuoka Pref. 4. Reproduction in the Japanese long-tailed field mouse, Apodemus argenteus. Journal of Mammalogical Society of Japan 5: 170-177.) and tits (Seki 2000Seki S-I (2000) A record of the third clutch of great tit in southern Japan. Strix 18: 145-148.). Notably, the varied tit, Parus varius (Temminck & Schlegel, 1845), occur as a third species of cavity breeders on that Island, although the effects of these tits on mice breeding may be negligible, in view of their differing breeding seasons (Ueta et al. 2007Ueta M, Seki S-I, Koike S (2007) Utility of a small temperature logger to monitor the breeding phenology at nest boxes of passerine bird species. Bird Research 3: T3-T11.) that do not overlap (Yoshida 1972Yoshida H (1972) Small mammals of Mt. Kiyomizu, Fukuoka Pref. 4. Reproduction in the Japanese long-tailed field mouse, Apodemus argenteus. Journal of Mammalogical Society of Japan 5: 170-177.).

Figure 2
Plots of the height of nest boxes used by Parus major and Apodemus argenteus with a logistic regression curve.

To avoid competition, sympatric cavity nesters often breed in the cavities in different seasons (Slagsvold 1978Slagsvold T (1978) Competition between the great tit Parus major and the pied flycatcher Ficedula hypoleuca: an experiment. Ornis Scandinavia 9: 46-50. https://doi.org/10.2307/3676138
https://doi.org/10.2307/3676138...
). Therefore, it is possible that mice avoid using boxes when breeding tits occupy them, to decrease competition, (Fig. 1). The mice are able to breed underground, as well as in cavities (Setoguchi 1981Setoguchi M (1981) Utilization of holes and home ranges in the Japanese long-tailed mice (Apodemus argenteus). Japanese Journal of Ecology 31: 385-394.). It is possible that, in this study area, mice breed underground from May to early July. Additional surveys are needed to examine the seasonal changes in the breeding sites of these mice.

ACKNOWLEDGMENTS

We thank T. Oshida and M.B. Takada for their constructive comments on this study. We also thank A. Kimoto for comments on statistical analyses. We acknowledge the invaluable comments of two anonymous reviewers and the editor on an earlier version of this manuscript.

LITERATURE CITED

  • Ando M (2005) Improvement of nest box investigation techniques for study of arboreal rodents. Mammalian Science 45: 165-176.
  • Czeszczewik D, Walankiewicz W, Stanska M (2008) Small mammals in nests of cavity-nesting birds: why should ornithologists study rodents? Canadian Journal of Zoology 86: 286-293. https://doi.org/10.1139/Z07-139
    » https://doi.org/10.1139/Z07-139
  • Fujimaki Y (1969) Reproductive activity in Apodemus argenteus Temminck. Journal of Mammalogical Society of Japan 4: 74-80.
  • Martin K, Aitken KEH, Wiebe KL (2004) Nest sites and nest webs for cavity-nesting communities in interior British Columbia, Canada: Nest characteristics and niche partitioning. Condor 106: 5-19. https://doi.org/10.1650/7482
    » https://doi.org/10.1650/7482
  • Martin K, Eadie JM (1999) Nest webs: A community-wide approach to the management and conservation of cavity-nesting forest birds. Forest Ecology and Management 115: 243-257. https://doi.org/10.1016/S0378-1127(98)00403-4
    » https://doi.org/10.1016/S0378-1127(98)00403-4
  • Minot EO, Perrins CM (1986) Interspecific interference competition - Nest-sites for Blue and Great tits. Journal of Animal Ecology 55: 331-350. https://doi.org/10.2307/4712
    » https://doi.org/10.2307/4712
  • Nakamura-Kojo Y, Kojo N, Tamate HB (2016) Spatial differences in arboreal activity of two rodents, the Japanese dormouse (Glirulus japonicus) and the small Japanese field mouse (Apodemus argenteus). Annals Zoologici Fenici 53: 81-92. https://doi.org/10.5735/086.053.0207
    » https://doi.org/10.5735/086.053.0207
  • Newton I (1994) The role of nest-sites in limiting the numbers of hole-nesting birds: a review. Biological Conservation 70: 265-276. https://doi.org/10.1016/0006-3207(94)90172-4
    » https://doi.org/10.1016/0006-3207(94)90172-4
  • R Core Team (2016) R: A language and environment for statistical computing. Vienna, R Foundation for Statistical Computing, https://www.R-project.org
    » https://www.R-project.org
  • Sakata T, Nakazono T, Kaoka H, Tanoue H, Amano M (2009) Confirmation of Japanese flying squirrel (Pteromys momonga) with nest boxes in Gokanosho and Naidaijin, Kumamoto Prefecture, Japan. Bulletin of Kumamoto Wildlife Society 5: 11-20.
  • Sakata T, Yasuda M, Nagamine S (2010) Confirmation of Japanese flying squirrel (Pteromys momonga) and Japanese dormouse (Glirulus japonicas) in Ookawa, Minamata city, Kumamoto prefecture, Japan. Bulletin of Kumamoto Wildlife Society 6: 23-28.
  • Seki S-I (2000) A record of the third clutch of great tit in southern Japan. Strix 18: 145-148.
  • Setoguchi M (1981) Utilization of holes and home ranges in the Japanese long-tailed mice (Apodemus argenteus). Japanese Journal of Ecology 31: 385-394.
  • Shafique CM, Barkati S, Oshida T, Ando M (2009) Comparison of nest trees of two sympatric flying squirrel species in northern Pakistan. Mammalian Biology 74: 240-244. https://doi.org/10.1016/j.mambio.2009.01.005
    » https://doi.org/10.1016/j.mambio.2009.01.005
  • Slagsvold T (1978) Competition between the great tit Parus major and the pied flycatcher Ficedula hypoleuca: an experiment. Ornis Scandinavia 9: 46-50. https://doi.org/10.2307/3676138
    » https://doi.org/10.2307/3676138
  • Suzuki K, Yanagawa H (2012) Different nest site selection of two sympatric arboreal rodent species, Siberian flying squirrel and small Japanese field mouse, in Hokkaido, Japan. Mammal Study 37: 243-247. https://doi.org/10.3106/041.037.0308
    » https://doi.org/10.3106/041.037.0308
  • Suzuki K, Yamane Y, Yanagawa H (2014) Nest site use by the small Japanese field mouse: possibility of nest height change in the presence of the Siberian flying squirrel. Mammalian Science 54: 243-249.
  • Suzuki K, Yamane Y, Yanagawa H (2016) Invasive cutleaf coneflower seeds cached in nest boxes: Possibility of dispersal by a native rodent. Plant Species Biology 31: 300-303. https://doi.org/10.1111/1442-1984.12115
    » https://doi.org/10.1111/1442-1984.12115
  • Ueta M, Seki S-I, Koike S (2007) Utility of a small temperature logger to monitor the breeding phenology at nest boxes of passerine bird species. Bird Research 3: T3-T11.
  • Yoshida H (1972) Small mammals of Mt. Kiyomizu, Fukuoka Pref. 4. Reproduction in the Japanese long-tailed field mouse, Apodemus argenteus Journal of Mammalogical Society of Japan 5: 170-177.
  • Yuta T, Koizumi I (2012) Long breeding season and high frequency of multiple brooding in great tits in Northern Japan. Ardea 100: 197-201. https://doi.org/10.5253/078.100.0211
    » https://doi.org/10.5253/078.100.0211
  • Editorial responsibility:

    Jorge Salazar-Bravo
  • Zoobank:

    http://zoobank.org/EDA3E6B1-D15B-451A-87D2-F912245A065C

Publication Dates

  • Publication in this collection
    2017

History

  • Received
    19 July 2016
  • Reviewed
    17 Oct 2016
  • Accepted
    10 Mar 2017
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