Despite a marked increase in the focus toward biodiversity conservation in fragmented landscapes, studies that confirm species breeding success are scarce and limited. In this paper, we asked whether local (area of forest patches) and landscape (amount of suitable habitat surrounding of focal patches) factors affect the breeding success of raccoon dogs (Nyctereutes procyonoides) in Tokyo, Central Japan. The breeding success of raccoon dogs is easy to judge as adults travel with pups during the breeding season. We selected 21 forest patches (3.3–797.8 ha) as study sites. In each forest patch, we used infra-red-triggered cameras for a total of 60 camera days per site. We inspected each photo to determine whether it was of an adult or a pup. Although we found adult raccoon dogs in all 21 forest patches, pups were found only in 13 patches. To estimate probability of occurrence and detection for raccoon in 21 forest fragments, we used single season site occupancy models in PRESENCE program. Model selection based on AIC and model averaging showed that the occupancy probability of pups was positively affected by patch area. This result suggests that large forests improve breeding success of raccoon dogs. A major reason for the low habitat value of small, isolated patches may be the low availability of food sources and the high risk of being killed on the roads in such areas. Understanding the effects of local and landscape parameters on species breeding success may help us to devise and implement effective long-term conservation and management plans.
Citation: Soga M, Koike S (2013) Large Forest Patches Promote Breeding Success of a Terrestrial Mammal in Urban Landscapes. PLoS ONE 8(1): e51802. https://doi.org/10.1371/journal.pone.0051802
Editor: Benedikt R. Schmidt, Universität Zurich, Switzerland
Received: July 11, 2012; Accepted: November 5, 2012; Published: January 2, 2013
Copyright: © 2013 Soga, Koike. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: This study was funded by Grant-in-Aid for Challenging Exploratory Research (22651086) and the Tokyu Foundation for Better Environment (no. 2012–13). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
Habitat fragmentation is now a global anthropogenic cause of biodiversity decline, and it has concerned many conservation biologists for a long time , . Previous studies – revealed that landscape configuration is important factors affecting species persistence in fragmented landscapes. Therefore, in fragmented landscapes, nature reserves with large, well-connected patches are preferred by many conservation biologists (e.g. ). Yet, current knowledge of the impact of fragmentation is largely limited to the probability of the occurrence of target species –. Studies that confirm factors affecting long-term species persistence (e.g. breeding success) are scarce , . Recent empirical studies  have demonstrated that several species occupying fragmented landscapes eventually disappeared without further fragmentation. Therefore, it is crucial to elucidate factors affecting breeding success of the target species . In this study, we asked whether both local and landscape forest cover affect the breeding success of raccoon dogs (Nyctereutes procyonoides) in a fragmented landscape, Tokyo, Central Japan. Raccoon dogs are an ideal model for determining breeding success because they interact with pups during the breeding season . In Japan, raccoon dogs are one of the most common mammals ,  and they play important roles in the forest ecosystem as seed dispersers  and predators . Therefore, conserving raccoon dogs is crucial for sustainable management of urban ecosystems.
Materials and Methods
1. Ethics Statement
In this study, we did not capture raccoon dogs. Thus, all work was legally conducted without acquiring a permit from the Tokyo Metropolitan Government or the Ministry of Environment of Japan.
2. Study area and sampling sites
The study region was located in the southwestern Tokyo, Central Japan (Fig. 1). The western boundary of the study area was formed by a mountain range dominated by Mount Takao (599 m above sea level). The forest patches were dominated by deciduous forests comprising two oak species, Quercus serrata Thunb. ex Murray and Q. acutissima Carruthers, along with Pinus densiflora Sieb. et Zucc., Abies firma Sieb. et Zucc. and the evergreen oaks, Q. glauca Thunb. ex Murray and Q. acuta Thunb. ex Murray. The border of a forest patch was defined as any treeless belt with an open canopy of more than 300 m. In Japan, a high number of raccoon dog roadkills (about 110,000–370,000 individuals) occur every year ; thus, we used roadways with more than 4 lanes as borders of forest patches. A total of 21 forest patches were selected that ranged widely in size (3.3–797.8 ha) (Fig. 1).
In this study, we used forest patch area and total forest area within 600 m from a focal patch as ‘local’ and ‘landscape’ variables, respectively. Other authors  stressed the positive influence of %forest cover within buffers. However, in this study, such an index had no significant effects on the breeding success of raccoon dogs, so we removed it from later analyses. Both local and landscape variables were calculated from detailed aerial photographs in 2011 (Geospatial Information Authority of Japan) using ArcView geographic information system software (ver. 3.2, ESRI, Redlands, CA).
3. Camera trapping
The presence of raccoon dogs in 21 forest patches was assessed from June to August 2011. Raccoon dogs bear pups in May and parents and pups move together a month later. Because pups leave their parents in September, we can determine whether raccoon dogs have succeeded in breeding by taking photographs of them from June to August (Fig. 2). In each forest patch and backyard site we set infra-red-triggered cameras (National Geographic Store, 5.0 Megapixel Infrared Digital Motion-detection Camera) for a total of 60 camera days per forest patch (3 cameras × continuous 20 days); all cameras had data packs that stamped each photograph with the time and date of the event. The time delay between photographs was set to a minimum of one minute. At each site, three camera traps were widely separated and were tied to a tree 50 cm above the ground. We placed camera traps in sites where the probability of raccoon dog detection was high (e.g. animal trails). We used tainted meats as bait. We checked each camera and changed batteries once a week. We entered the photographed data into a computer recording the frame number, date, time and species for each film. The species in each photo was identified and it was determined whether only adults were present or adults with pups (Fig. 2).
4. Statistical analysis
To estimate probability of occurrence (ψ) and detection (p) for raccoon in 21 forest fragments, we used single season site occupancy models  in PRESENCE . In the input spreadsheet, we inserted ‘1’ if the patch was occupied by individuals and ‘0’ if it was not occupied in a given day. In this study, we constructed nine models (Table 1) using both local and landscape variables as continuous variables. First, we held the probability of sites occupied constant, ψ(·), and allowed species detection to vary with each covariate, p(Local) and p(Landscape) (two models). Second, we held species detection probability constant, p(·), and variedψwith each covariate separately, ψ(Local) andψ(Landscape) (two models). Third, we combined ψ(·)p(Cov) model andψ(Cov)p(·) in aψ(Cov)p(Cov), ψ(Local)p(Local), ψ(Local)p(Landscape), ψ(Landscape)p(Local) andψ(Landscape)p(Landscape) (four models). Also, we used a constant model, ψ(·)p(·), as a reference (one model). These nine models were ranked according to the Akaike Information Criterion (AICc) calculated by program PRESENCE. We also performed model averaging to obtain estimates and associated standard errors for each parameter of interest . We repeated these procedures for both adults and pups (Table 1).
Results and Discussion
In total, 443 photographs were taken. Adult raccoon dogs were observed in all forest patches. The best model (Model 1 in adults) suggested that detection rates of adults were 61.9 ± 5.9 (mean ± SE) %. Although the model p(Local) was better than the reference model (ψ(·)p(·)), their AIC differences were only 0.95 (Table 1). Also, including the landscape variable in model never improved model fit. These results suggest that occurrence probability of adults were not explained by both local and landscape variables.
Unlike adults, pups did not occur in all forest patches. We detected pups at 61.9% (13 of 21) patches. The best model (Model 1 in pups) suggested that 65.6∓12.1% of patches were occupied by pups, with a detection rate of 28.5∓5.5%. By including the local variable in our estimates of both occupancy and detection probability, ψ(Local) and p(Local), we were always able to explain the detection probability of pups more explicitly compared to the reference model (Table 1). Based on model averaging, the occurrence probability of raccoon dogs increased strongly with the local variable (i.e. forest patch area; Table 2). The 95% CI of parameter estimates of the local variable did not include zero (Table 2). On the contrary, landscape variable never improved model fit (Table 1).
These results suggest that patch area positively affects the breeding success of raccoon dogs. In Japan, although raccoon dogs depend strongly on forests for foraging and breeding , they are considered to be insensitive to urbanization . However, our findings indicate that the long-term survival of several populations of raccoon dogs, especially those in small and isolated patches, is not guaranteed.
There are several possible reasons why we did not observe pups in small patches. First, they need a relatively large habitat area for their daily home range . Second, in small forest patches, the abundance of ground beetles, which are their main food source , was markedly decreased by synergistic interactions between area loss and edge effects . The breeding success of vertebrates generally depends on the abundance of food resources . However, in this study, the effect of landscape variable on reproductive success was not significant and weak. One possible reason of this is that the matrix environments surrounding our patches were completely urbanized. In urban areas, traffic roads are thought to have negative effects on the ability of species to migrate between patches . Therefore, long-distance movement across the urban matrix is also associated with a high roadkill risk . In fact, the annual raccoon dog roadkill rate in Japan is high and such accidents have a strong impact on the population dynamics and persistence of a species .
Determination of the effects of landscape parameters on species breeding success may help us to devise and implement effective long-term conservation and management plans. Clarifying how we should arrange many natural forest patches in fragmented landscapes before urbanization proceeds is crucial for preventing biodiversity loss worldwide and for managing forest ecosystems in urban landscapes.
Conceived and designed the experiments: MS SK. Performed the experiments: MS. Analyzed the data: MS. Contributed reagents/materials/analysis tools: MS SK. Wrote the paper: MS SK.
- 1. Kruess A, Tscharntke T (1994) Habitat fragmentation, species loss, and biological control. Science 264: 1581.
- 2. Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Annual Review of Ecol Evol Syst 34: 487–515.
- 3. Lomolino MV (1990) The target area hypothesis–the influence of island area on immigration rates of non-volant mammals. Oikos 57: 297–300.
- 4. Hanski I (1994) Patch-occupancy dynamics in fragmented landscapes. Trends Ecol Evol 9: 131–135.
- 5. Prugh LR, Hodges KE, Sinclair ARE, Brashares JS (2008) Effect of habitat area and isolation on fragmented animal populations. Proc Nad Acad Sci USA 105: 20770–20775.
- 6. Diamond JM (1975) The island dilemma: lessons of modern biogeographic studies for the design of natural reserves. Biol Conserv 7: 129–146.
- 7. Davies KF, Margules CR (1998) Effects of habitat fragmentation on carabid beetles: experimental evidence. J Anim Ecol 67: 460–471.
- 8. Kurosawa R, Askins RA (2003) Effects of habitat fragmentation on birds in deciduous forests in Japan. Conserv Biol 17: 695–707.
- 9. Mortelliti A, Amori G, Capizzi D, Cervone C, Fagiani S, et al. (2011) Independent effects of habitat loss, habitat fragmentation and structural connectivity on the distribution of two arboreal rodents. J Appl Ecol 48: 153–162.
- 10. Marzluff JM, Raphael MG, Sallabanks R (2000) Understanding the effects of forest management on avian species. Wildl Soc Bull 28: 1132–1143.
- 11. Newmark WD, Stanley TR (2011) Habitat fragmentation reduces nest survival in an Afrotropical bird community in a biodiversity hotspot. Proc Natl Acad Sci USA 108: 11488–11493.
- 12. Ford HA, Walters JR, Cooper CB, Debus SJS, Doerr VAJ (2009) Extinction debt or habitat change?-Ongoing losses of woodland birds in north-eastern New South Wales, Australia. Biol Conserv 142: 3182–3190.
- 13. Kurki S, Nikula A, Helle P, Lindén H (2000) Landscape fragmentation and forest composition effects on grouse breeding success in boreal forests. Ecology 81: 1985–1997.
- 14. Takatsuki S, Yamagiwa J (2008) Mammalogy in Japan. University of Tokyo Press, Tokyo.
- 15. Harashina K, Tsunekawa A, Takeuchi K, Takatsuki S (1999) Relationships between Connectivity of Forests and Distributions of Terrestrial Manlrnals in Honshu, Japan. J Japan Inst Landsc Archit 62: 569–572.
- 16. Sonoda Y, Kuramoto N (2002) The effect of landscape pattern on rescue data of raccoon dogs in subyrban area. Envir Syst Res 30: 101–107.
- 17. Koike S, Morimoto H, Goto Y, Kozakai C, Yamazaki K (2008) Frugivory of carnivores and seed dispersal of fleshy fruits in cool-temperate deciduous forests. J For Res 13: 215–222.
- 18. Kauhala K, Laukkanen P, Rége I (1998) Summer food composition and food niche overlap of the raccoon dog, red fox and badger in Finland. Ecography 21: 457–463.
- 19. Saeki M, Macdonald D (2004) The effects of traffic on the raccoon dog (Nyctereutes procyonoides viverrinus) and other mammals in Japan. Biol Conserv 118: 559–571.
- 20. Prugh LR (2009) An evaluation of patch connectivity measures. Ecol Appl 19: 1300–1310.
- 21. Hines JE (2006) PRESENCE2 – Software to estimate patch occupancy and related parameters. USGS-PWRC. Available: http://www.mbr-pwrc.usgs.gov/software/presence.html. (Accessed 2012 Nov 24.).
- 22. Ohdachi SD, Ishibashi Y, Iwasa MA, Saitoh T (2009) The wild mammals of Japan. Shoukadoh, Kokyo.
- 23. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information–theoretic approach. Second edition. Springer-Verlag, New York, New York, USA.
- 24. Sonoda Y, Kuramoto N (2008) Effect of forest fragmentation on species composition of non-flying mammals in the Tama hill and Kanto mountain region. Ecol Civ Eng 11: 41–49.
- 25. Hirasawa M, Kanda E, Takatsuki S (2006) Seasonal food habits of the raccoon dog at a western suburb of Tokyo. Mammal Study 31: 9–14.
- 26. Soga M, Kanno N, Yamaura Y, Koike S (in press) Patch size determines the strength of edge effects on carabid beetle assemblages in urban remnant forests. J Insect Conserv.
- 27. Morrison ML, Marcot BG, Mannan RW (1998) Wildlife-habitat relationships – concepts and applications. Island, Washington DC.
- 28. Mader HJ (1984) Animal habitat isolation by roads and agricultural fields. Biol Conserv 29: 81–96.