Vol. 76 (2) 2024

ARTICLES

Human Presence as a Factor Determining the Circadian Activity of Mammal Species in the Sinite Kamani Nature Park

Nikolay P. Dolapchiev1,*, Diana P. Zlatanova2, Dilian Georgiev3 & Elitsa D. Popova2

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*1Institute of Biodiversity and Ecosystem Research, Bulgarian Academy of Sciences, 2 Gagarin Street, 1113 Sofia, Bulgaria; E-mail: ndolapchiev@gmail.com
2Department of Zoology and Anthropology, Faculty of Biology, Sofia University “St. Kliment Ohridski”, 8 Dragan Tsankov Blvd., 1164 Sofia, Bulgaria; E-mail: dianazlatanova@biofac.uni-sofia.bg; elitsa.popova@uni-sofia.bg
3Plovdiv University “Paisii Hilendarski”, 24 Tsar Assen Street, 4000 Plovdiv, Bulgaria; E-mail: diliangeorgiev@gmail.com

https://doi.org/10.71424/azb76.2.002777

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Abstract
The circadian activity of selected mammal species and the temporal overlap with human presence or between species were analysed in 2013–2014 on the territory of the Sinite Kamani Nature Park, Eastern Stara Planina. The purpose of this study was to determine how the human presence affected the circadian activity of mammal species in this protected area. The wild boar (n = 68) showed 22% overlap with the humans (n = 54) in its circadian activity (Δ = 0.22, CI 0.02–0.21) while the roe deer (n = 144) activity overlapped in 49% with the human activity (Δ = 0.49, CI 0.29–0.51). The European brown hare (n=26) activity had a 23% overlap (Δ = 0.23, CI 0.07–0.26), the golden jackal (n = 42) – 36% (Δ = 0.36, CI 0.22–0.49) and the red fox (n = 131) – 24% (Δ = 0.24, CI 0.06–0.25). The overlap between the red fox and European brown hare activity was 81% (Δ = 0.81, CI 0.71–0.93), between red fox and golden jackal – 71% (Δ = 0.71, CI0.49–0.77) and between red fox and Martes sp. – 81% (Δ = 0.81, CI 0.72–0.93). The target species avoided the range of time when humans were active. This forced the species to use a narrower temporal niche when sharing the same space. These results provided insights for the better management of the species in the protected areas.

Key words
human disturbance, wild animals, protected area

How to Cite
Dolapchiev N.P., Zlatanova D.P., Georgiev D. & Popova E.D. 2024. Human Presence as a Factor Determining the Circadian Activity of Mammal Species in the Sinite Kamani Nature Park. Acta zoologica bulgarica 76 (2) 187-196.

References

  1. Arjo W. M. & Pletscher D. H. 1999. Behavioral responses of coyotes to wolf recolonization in northwestern Montana. Canadian Journal of Zoology 77 (12): 1919–1927; doi: 10.1139/z99-177
  2. Barrull J., Mate I., Ruiz-Olmo J., Casanovas J. G., Gosàlbez J. & Salicrú M. 2014. Factors and mechanisms that explain coexistence in a Mediterranean carnivore assemblage: An integrated study based on camera trapping and diet. Mammalian Biology 79 (2): 123–131; doi: 10.1016/j.mambio.2013.11.004
  3. Boitani L., Mattei L., Nonis D. & Corsi F. 1994. Spatial and activity patterns of wild boars in Tuscany, Italy. Journal of Mammalogy 75 (3): 600–612; doi: 10.2307/1382507
  4. Bulgarian Biodiversity Law [In Bulgarian] 2022. https://lex.bg/laws/ldoc/2135456926
  5. Caruso N., Valenzuela A. E. J., Burdett C. L., Luengos Vidal E. M., Birochio D. & Casanave E. B. 2018. Summer habitat use and activity patterns of wild boar Sus scrofa in rangelands of central Argentina. PLoS ONE 13 (10): 1–15; doi: 10.1371/journal.pone.0206513
  6. Cederlund G. 1989. Activity patterns in moose and roe deer in a north boreal forest. Holarctic Ecology 12 (1): 39–45; doi: 10.1111/j.1600-0587.1989.tb00820.x
  7. Clinchy M., Zanette L. Y., Roberts D., Suraci J. P., Buesching C. D., Newman C. & Macdonald D. W. 2016. Fear of the human “super predator” far exceeds the fear of large carnivores in a model mesocarnivore. Behavioral Ecology 27(6): 1826–1832. doi:10.1093/beheco/arw117
  8. Cole D. N. & Landres P. B. 1995. Indirect effects of recreation on wildlife. Wildlife and Recreationists: Coexistence through Management and Research: 183–202.
  9. Cordell H. K., Betz C. J. & Green G. T. 2008. Nature-based Outdoor Recreation Trends and Wilderness. International Journal of Wilderness 14 (2): 7–10.
  10. Creel S., Winnie J. A., Christianson D. & Liley S. 2008. Time and space in general models of antipredator response: tests with wolves and elk. Animal Behaviour 76 (4): 1139–1146; doi: 10.1016/j.anbehav.2008.07.006
  11. Cruz P., Iezzi M. E., De Angelo C., Varela D., Di Bitetti M. S. & Paviolo A. 2018. Effects of human impacts on habitat use, activity patterns and ecological relationships among medium and small felids of the Atlantic Forest. PLoS ONE 13 (8): 1–21; doi: 10.1371/journal.pone.0200806
  12. Czech B., Krausman P. R. & Devers P. K. 2000. Economic associations among causes of species endangerment in the United States. BioScience 50 (7): 593–601; doi: 10.1641/0006-3568(2000)050[0593:EAACOS]2.0.CO;2
  13. Darimont C. T., Red fox C. H., Bryan H. M. & Reimchen T. E. 2015. The unique ecology of human predators. Science 349 (6250): 858–860; doi: 10.1126/science.aac4249
  14. Dirzo R., Young H. S., Galetti M., Ceballos G., Nick J. B. & Collen B. 2014. Defaunation in the antropocene. Science 345 (6195): 401–406.
  15. Dolapchiev N. P., Zlatanova D. P., Popova E. D. & Chanev M. R. 2023a. Spatio-temporal analyses on roe deer activity (Capreolus capreolus L.) in areas with and without wolf (Canis lupus L.) presence. Ecologia Balkanica 15 (2): 1–11.
  16. Dolapchiev N., Popova E. & Zlatanova D. 2023b. Activity overlap and time-spacing between the wolf Canis lupus L. (Carnivora: Canidae) and its ungulate prey in Osogovo Mtn., Bulgaria. Acta Zoologica Bulgarica 75 (2): 215–224; https://www.acta-zoologica-bulgarica.eu/2023/002711.pdf
  17. Doykin N. 2018. Interspecies relationships in selected species of mammals on the territory of Vitosha Nature Park. Doctoral Dissertation. Sofia University ‘St. Kliment Ohridski’, Faculty of Biology, Department of Zoology and Anthropology. 144 p.
  18. Dröge E., Creel S., Becker M. S. & M’Soka J. 2017. Risky times and risky places interact to affect prey behaviour. Nature Ecology and Evolution 1 (8): 1123–1128; doi: 10.1038/s41559-017-0220-9
  19. Eriksen A., Wabakken P., Zimmermann B., Andreassen H. P., Arnemo J. M., Gundersen H., Liberg O., Linnell J., Milner J. M., Pedersen H. C., Sand H., Solberg E. J. & Storaas T. 2011. Activity patterns of predator and prey: A simultaneous study of GPS-collared wolves and moose. Animal Behaviour 81 (2): 423–431; doi: 10.1016/j.anbehav.2010.11.011
  20. Farkas A., Jánoska F., Fodor J. T. & Náhlik A. 2017. The high level of nutritional niche overlap between red fox (Vulpes vulpes) and sympatric golden jackal (Canis aureus) affects the body weight of juvenile red foxes. European Journal of Wildlife Research 63 (3): 2–5; doi: 10.1007/s10344-017-1101-x
  21. Fedriani J. M., Palomares F. & Delibes M. 1999. Niche relations among three sympatric Mediterranean carnivores. Oecologia 121 (1): 138–148; doi: 10.1007/s004420050915
  22. Finney S. K., Pearce-Higgins J. W. & Yalden D. W. 2005. The effect of recreational disturbance on an upland breeding bird, the golden plover Pluvialis apricaria. Biological Conservation 121 (1): 53–63; doi: 10.1016/j.biocon.2004.04.009
  23. Frid A. & Dill. L. M. 2002. Human-caused disturbance stimuli as a form of predation risk. Conservation Ecology 6 (1): 11.
  24. Gaynor K. M., Hojnowski C. E., Carter N. H. & Bras J. S. 2018. The influence of human disturbance on wildlife nocturnality. Science 360 (6394): 1232–1235; doi: 10.1126/science.aar7121
  25. Georgiev D., Mechev A., Stoeva E., Dilovski G. & Pavlova A. 2015. On the activity of two medium-sized canids : the golden jackal (Canis aureus) and the red fox (Vulpes vulpes) in the Natural Park “Sinite Kamani” (Bulgaria) revealed by camera traps. ZooNotes 69 (January 2014): 1–4.
  26. Hansen A. J., Knight R. L., Marzluff J. M., Powell S., Brown K., Gude P. H. & Jones K. 2005. Effects of exurban development on biodiversity: Patterns, mechanisms, and research needs. Ecological Applications 15 (6): 1893–1905; doi: 10.1890/05-5221
  27. Holley A. J. F. 2001. The day activity period of the European brown hare (Lepus europaeus). Mammalian Biology (66): 357–364.
  28. Homolka M. 1986. Daily activity pattern of the European brown hare (Lepus europaeus). Folia Zoologica (Zoologicke Listy) 35 (1): 33–42.
  29. Jeppesen J.-L. 1989. Activity patterns of free-ranging roe deer (Capreolus capreolus) at Kalo. Danish Review of Game Biology 13 (8): 1–32.
  30. Kamler J. F., Ballard W. B., Gilliland R. L. & Ii P. R. L. 2016. Impacts of Coyotes on Swift Red foxes in Northwestern Texas. 67 (2): 317–323; http://www.jstor.org/stable/3802773
  31. Kerley L. L., Goodrich J. M., Miquelle D. G., Smirnov E. N., Quigley H. B. & Hornocker M. G. 2002. Effects of roads and human disturbance on Amur tigers. Conservation Biology 16 (1): 97–108; doi: 10.1046/j.1523-1739.2002.99290.x
  32. Kohl M. T., Stahler D. R., Metz M. C., Forester J. D., Kauffman M. J., Varley N., White P. J., Smith D. W. & MacNulty D. R. 2018. Diel predator activity drives a dynamic landscape of fear. Ecological Monographs 88 (4): 638–652; doi: 10.1002/ecm.1313
  33. Lacy K. E. & Martins E. P. 2003. The effect of anthropogenic habitat usage on the social behaviour of a vulnerable species, Cyclura nubila. Animal Conservation 6 (1): 3–9; doi: 10.1017/S1367943003003020
  34. Lange P. N. A. M. J. G., Lelieveld G. & De Knegt H. J. 2021. Diet composition of the golden jackal Canis aureus in south-east Europe – a review. Mammal Review 51 (2): 207–213; doi: 10.1111/mam.12235
  35. Lanszki J., Kurys A., Szabó L., Nagyapáti N., Porter L. B. & Heltai M. 2016. Diet composition of the golden jackal and the sympatric red fox in an agricultural area (Hungary). Folia Zoologica 65 (4): 310–322; doi: 10.25225/fozo.v65.i4.a3.2016
  36. Larson C., Dertien J. S., Larson C. L. & Reed S. E. 2021. Recreation effects on wildlife: a review of potential quantitative thresholds. Americas Program, Wildlife Conservation Society, 1474.
  37. Larson C. L., Reed S. E., Merenlender A. M. & Crooks K. R. 2016. Effects of recreation on animals revealed as widespread through a global systematic review. PLoS ONE 11 (12): 1–21; doi: 10.1371/journal.pone.0167259
  38. Law on Protected Areas 1998. State Gazette No. 133/1998 (In Bulgarian).
  39. Liu X., Wu P., Songer M., Cai Q., He X., Zhu Y. & Shao X. 2013. Monitoring wildlife abundance and diversity with infra-red camera traps in Guanyinshan Nature Reserve of Shaanxi Province, China. Ecological Indicators 33: 121–128; doi: 10.1016/j.ecolind.2012.09.022
  40. Magle S., Zhu J. & Crooks K. R. 2005. Behavioral responses to repeated human intrusion by black-tailed prairie dogs (Cynomys ludovicianus). Journal of Mammalogy 86 (3): 524–530; doi: 10.1644/1545-1542(2005)86[524:BRTRHI]2.0.CO;2
  41. Mainini B., Neuhaus P. & Ingold P. 1993. Behaviour of marmots Marmota marmota under the influence of different hiking activities. Biological Conservation 64 (2): 161–164; https://doi.org/10.1016/0006-3207(93)90653-I
  42. Markov G. & Lanszki J. 2012. Diet composition of the golden jackal, Canis aureus in an agricultural environment. Folia Zoologica 61 (1): 44–48; doi: 10.25225/fozo.v61.i1.a7.2012
  43. Meredith M. 2022. Package ‘overlap’ – Estimates of Coefficient of Overlapping for Animal Activity Patterns.
  44. Moreira-Arce D., Vergara P. M. & Boutin S. 2015. Diurnal human activity and introduced species affect occurrence of carnivores in a human-dominated landscape. PLoS ONE 10 (9): 1–19; doi: 10.1371/journal.pone.0137854
  45. Mori E., Bagnato S., Serroni P., Sangiuliano A., Rotondaro F., Marchianò V., Cascini V., Poerio L. & Ferretti F. 2020. Spatiotemporal mechanisms of coexistence in an European mammal community in a protected area of southern Italy. Journal of Zoology 310 (3): 232–245; doi: 10.1111/jzo.12743
  46. Natural Park Sinite Kamani (not dated). https://dppsk.org/en/inanimate-nature-climate/
  47. Packard J. M., Clemmons J. R. & Buchholz R. 1999. Behavioral approaches to conservation in the wild. Journal of Wildlife Management 63 (1): 411; doi: 10.2307/3802529
  48. Pagon N., Grignolio S., Pipia A., Bongi P., Bertolucci C. & Apollonio M. 2013. Seasonal variation of activity patterns in roe deer in a temperate forested area. Chronobiology International 30 (6): 772–785; doi: 10.3109/07420528.2013.765887
  49. Pepin D. & Cargnelutti B. 1994. Individual variations of daily activity patterns in radiotracked European brown hares during winter. Acta Theriologica 39 (4): 399–409; doi: 10.4098/at.arch.94-46
  50. Petrov A. E. 2022. On the circadian activity of red fox (Vulpes vulpes) and stone marten (Martes foina) in agricultural landscape of Northwestern Bulgaria during spring-summer period. Ecologia Balkanica 14 (2): 205–208.
  51. Petrov P. R., Popova E. D. & Zlatanova D. P. 2016. Niche partitioning among the red fox Vulpes vulpes (L.), stone marten Martes foina (Erxleben) and pine marten Martes martes (L.) in two mountains in Bulgaria. Acta Zoologica Bulgarica 68 (3): 375–390.
  52. Popov V. 2007. Terrestrial mammals of Bulgaria: Zoogeographical and Ecological Patterns of Distribution. Biogeography and Ecology of Bulgaria. In: Fet V. & Popov A. (Eds): Biogeography and Ecology of Bulgaria. Monographiae Biologicae, vol. 82. Springer, Dordrecht. https://doi.org/10.1007/978-1-4020-5781-6_2
  53. Popova E. D., Zlatanova D. P. & Todev V. 2017. Diversity and temporal relationships between mammals at feeding stations in Western Rhodope Mountains, Bulgaria. Acta Zoologica Bulgarica 69 (4): 529–540.
  54. Posillico M., Serafini P. & Lovari S. 1995. Activity patterns of the stone marten Martes foina Erxleben, 1777, in relation to some environmental factors. Hystrix, the Italian Journal of Mammalogy 7 (1–2): 79–97; doi: 10.4404/hystrix-7.1-2-4056
  55. Racheva V., Zlatanova D., Peshev D. & Markova E. 2012. Camera traps recorded use of sett sites by badgers (Meles meles L., Мammalia) in different habitats. Acta Zoologica Bulgarica 64 (2): 145–150.
  56. Raichev E. 2018. Determination of Stone marten (Martes foina) and Pine marten (Martes martes) in natural habitats using camera traps. Agricultural Science and Technology 10 (2): 160–163; doi: 10.15547/ast.2018.02.031
  57. Ridout M. S. & Linkie M. 2009. Estimating overlap of daily activity patterns from camera trap data. Journal of Agricultural, Biological and Environmental Statistics 14 (3): 322–337; doi: 10.1198/jabes.2009.08038
  58. Ripple W. J., Estes J. A., Beschta R. L., Wilmers C. C., Ritchie E. G., Hebblewhite M., Berger J., Elmhagen B., Letnic M., Nelson M. P., Schmitz O. J., Smith D. W., Wallach A. D. & Wirsing A. J. 2014. Status and ecological effects of the world’s largest carnivores. Science 343 (6167); doi: 10.1126/science.1241484
  59. Rodríguez-Prieto I. & Fernández-Juricic E. 2005. Effects of direct human disturbance on the endemic Iberian frog Rana iberica at individual and population levels. Biological Conservation 123 (1): 1–9; doi: 10.1016/j.biocon.2004.10.003
  60. Russo L., Massei G. & Genov P. V. 1997. Daily home range and activity of wild boar in a Mediterranean area free from hunting. Ethology Ecology and Evolution 9 (3): 287–294; doi: 10.1080/08927014.1997.9522888
  61. Scheinin S., Yom-Tov Y., Motro U. & Geffen E. 2006. Behavioural responses of red foxes to an increase in the presence of golden jackals: A field experiment. Animal Behaviour 71 (3): 577–584; doi: 10.1016/j.anbehav.2005.05.022
  62. Serafini P. & Lovari S. 1993. Food habits and trophic niche overlap of the red fox and the stone marten in a Mediterranean rural area. Acta Theriologica 38 (3): 233–244; doi: 10.4098/AT.arch.93-19
  63. Smith J. A., Suraci J. P., Clinchy M., Crawford A., Roberts D., Zanette L. Y. & Wilmers C. C. 2017. Fear of the human ‘super predator’ reduces feeding time in large carnivores. Proceedings of the Royal Society. B: Biological Sciences 284 (1857); doi: 10.1098/rspb.2017.0433
  64. Sporek M. 2017. Monitoring of 24-hours activity in a population of wild boar (Sus scrofa). Ecological Chemistry and Engineering A 24 (2): 277–283; doi: 10.2428/ecea.2017.24(2)20
  65. Stolle K., van Beest F. M., Vander Wal E. & Brook R. K. 2015. Diurnal and nocturnal activity patterns of invasive. The Canadian Field-Naturalist 129: 76–79.
  66. Suraci J. P., Clinchy M., Zanette L. Y. & Wilmers C. C. 2019a. Fear of humans as apex predators has landscape-scale impacts from mountain lions to mice. Ecology Letters 22 (10): 1578–1586; doi: 10.1111/ele.13344
  67. Suraci J. P., Frank L. G., Oriol-Cotterill A., Ekwanga S., Williams T. M. & Wilmers C. C. 2019b. Behavior-specific habitat selection by African lions may promote their persistence in a human-dominated landscape. Ecology 100 (4): 1–11; doi: 10.1002/ecy.2644
  68. Tablado Z. & Jenni L. 2017. Determinants of uncertainty in wildlife responses to human disturbance. Biological Reviews 92 (1): 216–233; doi: 10.1111/brv.12224
  69. Tsunoda H., Ito K., Peeva S., Raichev E. & Kaneko Y. 2018. Spatial and temporal separation between the golden jackal and three sympatric carnivores in a human-modified landscape in central Bulgaria. Zoology and Ecology 28 (3): 172–179; doi: 10.1080/21658005.2018.1504406
  70. Tsunoda H., Newman C., Peeva S., Raichev E., Buesching C. D. & Kaneko Y. 2020. Spatio-temporal partitioning facilitates mesocarnivore sympatry in the Stara Planina Mountains, Bulgaria. Zoology 141: 125801; doi: 10.1016/j.zool.2020.125801
  71. Tsunoda H., Peeva S., Raichev E., Kronawetter T., Kirilov K. B., Georgiev D. & Kaneko Y. 2022. Patterns of spatial distribution and diel activity in carnivore guilds (Carnivora). Journal of Vertebrate Biology 71, 22018; doi: 10.25225/jvb.22018
  72. Tucker M. A., Böhning-Gaese K., Fagan W. F., Fryxell J. M., Van Moorter B., Alberts S. C., Ali A. H., Allen A. M., Attias N., Avgar T. & Bartlam-Brooks H. 2018. Moving in the Anthropocene: Global reductions in terrestrial mammalian movements. Science 359 (6374): 466–469.
  73. Vlasseva A., Chassovnikarova T. & Atanassov N. 2017. Autumn-winter diet and food niche overlap between red fox (Vulpes vulpes L., 1758) and golden jackal (Canis aureus L., 1758) in two regions in Bulgaria. Acta Zoologica Bulgarica, Suppl. 8: 217–220.
  74. Wallach A. D., Shanas U. & Inbar M. 2010. Feeding activity and dietary composition of roe deer at the southern edge of their range. European Journal of Wildlife Research 56 (1): 1–9; doi: 10.1007/s10344-009-0281-4
  75. Yalden P. E. & Yalden D. W. 1988. The level of recreational pressure on blanket bog in the Peak District National Park, England. Biological Conservation 44 (3): 213–227; doi: 10.1016/0006-3207(88)90103-6
  76. Yalden P. E. & Yalden D. W. 1990. Recreational disturbances of breeding golden plovers Pluvialis apricarius. Biological Conservation 51 (4): 243–262; doi: 10.1016/0006-3207(90)90111-2
  77. Zalewski A. 2006. Factors affecting the duration of activity by pine martens (Martes martes) in the Białowieża National Park, Poland. Journal of Zoology 251(4): 439–447.
  78. Zielinski W. J., Spencer W. D. & Barrett R. H. 1983. Relationship between food habits and activity patterns of pine marten. Journal of Mammalogy 64 (3): 387–396; doi: 10.2307/1380351