Behavioral island syndrome and its ecological drivers in the Mednyi Island Arctic fox

Cover Page

Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription Access

Abstract

Reptiles, birds, and mammals inhabiting oceanic islands tend to change many ecological, behavioral, and genetic characteristics. These changes are referred to as the “island syndrome”. The behavioral components of these changes have been little studied so far. Based on a 40-year study of the biology of the Arctic fox (Vulpes lagopus) on the Mednyi Island, we show that the island Arctic foxes changed many behavioral characteristics compared to mainland foxes. They use smaller home ranges, travel shorter daily distances, and their dispersal distance from the natal territory is much smaller. An increase in the family size of the island Arctic foxes, together with a decrease in litter size, leads to an increase in parental and kin investment and increased cooperation between family members. At the same time, the island foxes, to a large extent, lost their fear of humans. These features are consistent with those found in other island populations. On the other hand, in contrast to other island populations, Mednyi Arctic foxes have increased territoriality, apparently in response to an increased risk of infanticide. Furthermore, Mednyi Arctic foxes expose sex-biased dispersal and maternal inheritance of home range, which are absent in the mainland foxes. The sex-biased dispersal can be considered a mechanism for avoiding inbreeding. Comparison with island fox (Urocyon littoralis) populations in the Channel Islands (Southern California) suggests that these traits have evolved under the influence of specific environmental drivers of the Mednyi Island: patchy and highly predictable resource distribution. The particular resource distribution led to the increased importance of another driver, social landscape, and a new behavioral metatrait of the Mednyi fox – increased conservatism in spatial, reproductive, and foraging behavior.

About the authors

M. E. Goltsman

Lomonosov Moscow State University, Biological Faculty, Department of Vertebrate Zoology

Author for correspondence.
Email: migolts@gmail.com
Russia, 119234, Moscow, Leninskie Gory, 1, Bldg. 12

E. P. Kruchenkova

Lomonosov Moscow State University, Biological Faculty, Department of Vertebrate Zoology

Email: doronina@uni-muenster.de
Russia, 119234, Moscow, Leninskie Gory, 1, Bldg. 12

L. O. Doronina

Institute of Experimental Pathology, ZMBE, University of Muеnster

Author for correspondence.
Email: doronina@uni-muenster.de
Germany, D-48149, Muenster, Von-Esmarch-Str., 56

References

  1. Бочарова Н.А., Гольцман М.Е., 2008. Микроскопическое исследование кожного покрова песца о‑ва Медный (Alopex lagopus semenovi Ognev, 1931) // Сохранение биоразнообразия Камчатки и прилегающих морей: Мат-лы IX междунар. научн. конф. 25–26 ноября 2008 г. Петропавловск-Камчатский: Изд-во “Камчатпресс”. С. 250–253.
  2. Ванисова Е.А., Никольский А.А., 2012. Биологическое сигнальное поле млекопитающих (к 110-летию со дня рождения профессора Н.П. Наумова) // Журн. общ. биологии. Т. 73. № 6. С. 403–417.
  3. Гептнер В.Г., 1967. Песец Alopex lagopus Linnaeus, 1758. Географическая изменчивость // Млекопитающие Советского Союза. Т. 2. Ч. 1. М.: Высш. шк. С. 205–208.
  4. Гольцман М.Е., Крученкова Е.П., Сергеев С.Н., Володин И.А., 2003. Песец острова Медного (Alopex lagopus semenovi). Особенности экологии островной популяции // Зоол. журн. Т. 82. № 4. С. 514–524.
  5. Гольцман М.Е., Нанова О.Г., Сергеев С.Н., Шиенок А.Н., 2010. Использование кормовых ресурсов репродуктивными семьями песцов (Alopex lagopus semenovi) на острове Медный (Командорские острова) // Зоол. журн. Т. 89. № 10. С. 1246–1263.
  6. Гольцман М.Е., Сушко Е.Д., Доронина Л.О., Крученкова Е.П., 2018. Индивидуум ориентированная модель популяционной динамики песца (Vulpes lagopus semenovi) на о-ве Медном (Командорские острова) // Зоол. журн. Т. 97. № 11. С. 1400–1417.
  7. Дарвин Ч., 1941. Путешествие натуралиста вокруг света на корабле “Бигль”. М.: Изд-во АН СССР. 618 с.
  8. Джикия Е.Л., Колесников А.А., Чудакова Д.А., Загребельный С.В., Гольцман М.Е., 2007. Генетический полиморфизм командорских популяций песцов (Alopex lagopus semenovi Ognev, 1931, Alopex lagopus beringensis Merriam, 1902) // Генетика. Т. 43. № 9. С. 1239–1245.
  9. Ильина Е.Д., 1950. Островное звероводство. М.: Международная книга. 302 с.
  10. Крученкова Е.П., Гольцман М.Е., 1994. Родительское поведение песца (Alopex lagopus semenovi) на острове Медном. Факторы, определяющие связь взрослых песцов и детенышей // Зоол. журн. Т. 73. № 5. С. 88–103.
  11. Крученкова Е.П., Гольцман М.Е., Фроммольт К.-Х., 2003. Ритмическая организация сериального лая песца: половозрастные и контекстные определяющие // Зоол. журн. Т. 82. № 4. С. 525–533.
  12. Мамаев Е.Г., 2010. Фауна китообразных акватории Командорских островов: ретроспективный анализ и современное состояние // Исследования водных биологических ресурсов Камчатки и северо-западной части Тихого океана. Вып. 19. С. 25–49.
  13. Нанова О.Г., 2021. Сопоставление морфологической дифференциации командорских песцов (Vulpes lagopus semenovi, Vulpes lagopus beringensis) с межвидовым уровнем различий в родах Urocyon и Vulpes (Canidae) // Зоол. журн. Т. 100. № 5. С. 573–589.
  14. аумов H.П., 1948. Очерки сравнительной экологии мышевидных грызунов. М.; Л.: Изд-во АН СССР. 204 с
  15. Наумов Н.П., 1972. Уровни организации живой материи и популяционная биология // Журн. общ. биологии. Т. 32. № 6. С. 651–666.
  16. Наумов Н.П., Голъцман М.Е., Крученкова Е.П., Овсяников Н.Г., Попов С.В., Смирин В.М., 1981. Социальное поведение песца на о. Медном. Факторы, определяющие пространственно-временной режим активности // Экология, структура популяций и внутривидовые коммуникативные процессы у млекопитающих. М.: Наука. С. 31–75.
  17. Никольский А.А., Рожнов В.В., Поярков А.Д., Михеев А.В., Авилова К.В. и др., 2013. Биологическое сигнальное поле млекопитающих. М.: Т-во науч. изд. КМК. 323 с.
  18. Овсяников Н.Г., 1993. Поведение и социальная организация песца. М.: Изд-во ЦНИЛ. 243 с.
  19. Огнев С.И., 1931. Звери Восточной Европы и Северной Азии. Т. 2. М.; Л.: ГЛАВНАУКА. 776 с.
  20. Плетенёв А.А., 2017. Использование участка обитания песцом (Vulpes lagopus beringensis, Merriam 1902) в период размножения. Магистерская дисс. М.: МГУ. 78 с.
  21. Пономарева Е.О., Исаченкова Л.Б., 1991. Общая физико-географическая характеристика Командорских островов // Природные ресурсы Командорских островов. М.: Изд-во МГУ. С. 17–29.
  22. Сдобников В.М., 1940. Опыт массового мечения песцов // Проблемы Арктики. № 12. Л.: Изд-во Главсевморпути. С. 106–110.
  23. Стеллер Г.В., 1995. Дневник плавания с Берингом к берегам Америки 1741–1742. М.: Изд. ПАN. 224 с.
  24. Цалкин В.И., 1944. Географическая изменчивость в строении черепа песцов Евразии // Зоол. журн. Т. 23. № 4. С. 156–169.
  25. Черский А.И., 1920. Командорский песец. Материалы по изучению рыболовства и пушного промысла на Дальнем Востоке. Токио: Изд. Управления Рыб. и Мор. Звер. промыслами. Вып. 1. С. 60–107.
  26. Шиляева Л.М., 1971. Экология и основы прогнозирования численности песца на примере североевропейской популяции. Дисс. … канд. биол. наук. Киров: ВНИИОЗ. 230 с.
  27. Adler G.H., Levins R., 1994. The island syndrome in rodent populations // Q. Rev. Biol. V. 69. P. 473–490.
  28. Anthony R.M., 1997. Home ranges and movements of Arctic fox (Alopex lagopus) in western Alaska // Arctic. V. 50. P. 147–157.
  29. Baier F., Hoekstra H.E., 2019. The genetics of morphological and behavioural island traits in deer mice // Proc. Roy. Soc. B. Biol. Sci. V. 286. № 1914. https://doi.org/10.1098/rspb.2019.1697
  30. Benítez-López A., Santini L., Gallego-Zamorano J., Milá B., Walkden P., et al., 2021. The island rule explains consistent patterns of body size evolution in terrestrial vertebrates // Nat. Ecol. Evol. V. 5. № 6. P. 768–786. https://doi.org/10.1038/s41559-021-01426-y
  31. Blanco G., Laiolo P., Fargallo J.A., 2014. Linking environmental stress, feeding-shifts and the “island syndrome”: A nutritional challenge hypothesis // Popul. Ecol. V. 56. № 1. P. 203–216.https://doi.org/10.1007/s10144-013-0404-3
  32. Buxton V.L., Enos J.K., Sperry J.H., Ward M.P., 2020. A review of conspecific attraction for habitat selection across taxa // Ecol. Evol. V. 10. № 23. P. 12690–12699. https://doi.org/10.1002/ece3.6922
  33. Clutton-Brock T., 1989. Female transfer and inbreeding avoidance in mammals // Nature. V. 337. P. 70–71. https://doi.org/10.1038/337070a0
  34. Clutton-Brock T., Sheldon B.C., 2010. Individuals and populations: the role of long-term, individual-based studies of animals in ecology and evolutionary biology // Trends Ecol. Evol. V. 25. № 10. P. 562–573.https://doi.org/10.1016/j.tree.2010.08.002
  35. Coonan T.J., Schwemm C.A., Garcelon D.K., Munson L., Assa Ch., 2010. Decline and Recovery of the Island Fox: A Case Study for Population Recovery. Cambridge; N.-Y.: Cambridge Univ. Press. 212 p.
  36. Creel S., 1998. Social organization and effective population size in carnivores // Behavioral Ecology and Conservation Biology / Ed. Caro T. Oxford: Oxford Univ. Press. P. 246–270.
  37. Crespin L., Duplantier J.-M., Granjon L., 2012. Demographic aspects of the island syndrome in two Afrotropical Mastomys rodent species // Acta Oecol. V. 39. P. 72–79. https://doi.org/10.1016/j.actao.2012.01.002
  38. Crook J.H., 1965. The adaptive significance of avian social organizations // Symp. Zool. Soc. Lond. V. 14. P. 181–218.
  39. Crooks K., 1994. Demography and status of the island fox and the island spotted skunk on Santa Cruz Island, California // Southwest. Nat. V. 39. № 3. P. 257–262. https://doi.org/10.2307/3671590
  40. Cypher B.L., Madrid A.Y., Van Horn Job C.L., Kelly E.C., Harrison S.W.R., Westall T.L., 2014. Multi-population comparison of resource exploitation by island foxes: Implications for conservation // Glob. Ecol. Conserv. V. 2. P. 255–266. https://doi.org/10.1016/j.gecco.2014.10.001
  41. Dalen L., Fuglei E., Hersteinsson P., Kapel C.M.O., Roth J.D., et al., 2005. Population history and genetic structure of a circumpolar species: the arctic fox // Biol. J. Linn. Soc. V. 84. P. 79–89. https://doi.org/10.1111/j.1095-8312.2005.00415.x
  42. Dobson F.S., 1982. Competition for mates and predominant juvenile male dispersal in mammals // Anim. Behav. V. 30. P. 1183–1192. https://doi.org/10.1016/S0003-3472(82)80209-1
  43. Dobson F.S., 2013. The enduring question of sex-biased dispersal: Paul J. Greenwood’s (1980) seminal contribution // Anim. Behav. V. 85. № 2. P. 299–304. https://doi.org/10.1016/j.anbehav.2012.11.014
  44. Ehrich D., Carmichael L., Fuglei E., 2011. Age-dependent genetic structure of arctic foxes in Svalbard // Polar Biol. V. 35. № 1. P. 53–62. https://doi.org/10.1007/s00300-011-1030-1
  45. Eide N.E., Stien A., Prestrud P., Yoccoz N.G., Fuglei E., 2011. Reproductive responses to spatial and temporal prey availability in a coastal Arctic fox population // J. Anim. Ecol. V. 81. № 3. P. 640–648.https://doi.org/10.1111/j.1365-2656.2011.01936.x
  46. Fernández-Palaciosa J.M., Kreft H., Irl S.D.H., Norderd S., Ah-Penge C., et al., 2021. Scientists’ warning – The outstanding biodiversity of islands is in peril // Glob. Ecol. Conserv. V. 31. https://doi.org/10.1016/j.gecco.2021.e01847
  47. Formica V.A., Tuttle E.M., 2009. Examining the social landscapes of alternative reproductive strategies // J. Evol. Biol. V. 22. № 12. P. 2395–2408.https://doi.org/10.1111/j.1420-9101.2009.01855.x
  48. Foster J., 1964. Evolution of mammals on islands // Nature. V. 202. № 4929. P. 234–235. https://doi.org/10.1038/202234a0
  49. Fraford K., Prestrud P., 1992. Home range and movements of arctic foxes Alopex lagopus in Svalbard // Polar Biol. V. 12. P. 519–526. https://doi.org/10.1007/BF00238191
  50. Fuglei E., Tarroux A., 2019. Arctic fox dispersal from Svalbard to Canada: One female’s long run across sea ice // Polar Res. V. 38. https://doi.org/10.33265/polar.v38.3646
  51. Funk W.C., Lovich R.E., Hohenlohe P.A., Hofman C.A., Morrison S.A., et al., 2016. Adaptive divergence despite strong genetic drift: genomic analysis of the evolutionary mechanisms causing genetic differentiation in the island fox (Urocyon littoralis) // Mol. Ecol. V. 25. № 10. P. 2176–2194.https://doi.org/10.1111/mec.13605
  52. Gavriilidi I., Meester G., de, Damme R., van, Baeckens S., 2022. How to behave when marooned: The behavioural component of the island syndrome remains underexplored // Biol. Lett. V. 18. https://doi.org/10.1098/rsbl.2022.0030
  53. Geffen E., Waidyaratne S., Dalén L., Angerbjörn A., Vila C., et al., 2007. Sea ice occurrence predicts genetic isolation in the Arctic fox // Mol. Ecol. V. 16. № 20. P. 4241–4255.https://doi.org/10.1111/j.1365-294x.2007.03507.x
  54. Gibson L.A., Cowana M.A., Lyons M.N., Palmer R., Pearson D.J., Doughty P., 2017. Island refuges: Conservation significance of the biodiversity patterns resulting from ‘natural’ fragmentation // Biol. Conserv. V. 212. P. 349–356. https://doi.org/10.1016/j.biocon.2017.06.010
  55. Goltsman M., Kruchenkova E.P., Sergeev S., Volodin I.A., Macdonald D.W., 2005a. “Island syndrome” in a population of Arctic foxes (Alopex lagopus) from Mednyi Island // J. Zool. V. 267. № 4. P. 405–418.
  56. Goltsman M., Kruchenkova E.P., Sergeev S., Johnson P.J., Macdonald D.W., 2005b. Effects of food availability on dispersal and cub sex ratios in the Mednyi arctic foxes, Alopex lagopus semenovi // Behav. Ecol. Sociobiol. V. 59. P. 198–206.
  57. Greenwood P.J., 1980. Mating systems, philopatry and dispersal in birds and mammals // Anim. Behav. V. 28. P. 1140–1162.
  58. Grenier-Potvin A., Clermont J., Gauthier G., Berteaux D., 2021. Prey and habitat distribution are not enough to explain predator habitat selection: addressing intraspecific interactions, behavioural state and time // Mov. Ecol. V. 9. № 12. https://doi.org/10.1186/s40462-021-00250-0
  59. Johnson D.D., Kays R., Blackwell P.G., Macdonald D.W., 2002. Does the resource dispersion hypothesis explain group living? // Trends Ecol. Evol. V. 17. P. 563–570. https://doi.org/10.1016/S0169-5347(02)02619-8
  60. Kruchenkova E.P., Goltsman M., Sergeev S., Macdonald D.W., 2009. Is alloparenting helpful for Mednyi Island arctic foxes, Alopex lagopus semenovi? // Naturwissenschaften. V. 96. № 4. P. 457–466. https://doi.org/10.1007/s00114-008-0494-5
  61. Lai S., Bêty J., Berteaux D., 2017. Movement tactics of a mobile predator in a meta-ecosystem with fluctuating resources: the arctic fox in the High Arctic // Oikos. V. 126. № 7. P. 937–947.https://doi.org/10.1111/oik.03948
  62. Lawson Handley L.J., Perrin N., 2007. Advances in our understanding of mammalian sex-biased dispersal // Mol. Ecol. V. 16. № 8. P. 1559–1578.https://doi.org/10.1111/j.1365-294x.2006.03152.x
  63. Li X.-Y., Kokko H., 2018. Sex-biased dispersal: A review of the theory // Biol. Rev. V. 94. № 2. P. 721–736. https://doi.org/10.1111/brv.12475
  64. Li X.-Y., Kokko H., 2019. Intersexual resource competition and the evolution of sex-biased dispersal // Front. Ecol. Evol. V. 7. https://doi.org/10.3389/fevo.2019.00111
  65. MacArthur R.H., Wilson E.O., 1963. An equilibrium theory of insular zoogeography // Evolution. V. 17. № 4. P. 373–387. https://doi.org/10.2307/2407089
  66. McNab B.K., 1994. Energy conservation and the evolution of flightlessness in birds // Am. Nat. V. 144. № 4. P. 628–642. https://doi.org/www.jstor.org/stable/2462941
  67. Norén K., Hersteinsson P., Samelius G., Eide N.E., Fuglei E., et al., 2012. From monogamy to complexity: Arctic fox social organization in contrasting ecosystems // Can. J. Zool. V. 90. P. 1102–1116. https://doi.org/10.1139/z2012-077
  68. O’Connor E.A., Cornwallis C.K., Hasselquist D., Nilsson J.A., Westerdahl H., 2018. The evolution of immunity in relation to colonization and migration // Nat. Ecol. Evol. V. 2. P. 841–849. https://doi.org/10.1038/s41559-018-0509-3
  69. Parmenter M.D., Nelson J.P., Gray M.M., Weigel S., Vinyard C.J., Payseur B.A., 2022. A complex genetic architecture underlies mandibular evolution in big mice from Gough Island // Genetics. V. 220. № 4. https://doi.org/10.1093/genetics/iyac023
  70. Pletenev A., Kruchenkova E., Mikhnevich Y., Roznov V., Goltsman M., 2021. The overabundance of resources leads to small but exclusive home ranges in Arctic fox (Vulpes lagopus) on Bering Island // Polar Biol. V. 44. P. 1427–1443. https://doi.org/10.1007/s00300-021-02888-3
  71. Ploshnitsa A.I., Goltsman M.E., Macdonald D.W., Kennedy L.J., Sommer S., 2012. Impact of historical founder effects and a recent bottleneck on MHC variability in Commander Arctic foxes (Vulpes lagopus) // Ecol. Evol. V. 2. № 1. P. 165–180.https://doi.org/10.1002/ece3.42
  72. Ploshnitsa A.I., Goltsman M.E., Happ G.M., Macdonald D.W., Kennedy L J., 2013. Historical and modern neutral genetic variability in Mednyi Arctic foxes passed through a severe bottleneck // J. Zool. V. 289. № 1. P. 68–76. https://doi.org/10.1111/j.1469-7998.2012.00964.x
  73. Poulin M., Clermont J., Berteaux D., 2021. Extensive daily movement rates measured in territorial arctic foxes // Ecol. Evol. V. 11. № 6. P. 2503–2514. https://doi.org/10.1002/ece3.7165
  74. Renaud S., Auffray J.-C., 2010. Adaptation and plasticity in insular evolution of the house mouse mandible // J. Zool. Syst. Evol. Res. V. 48. № 2. P. 138–150. https://doi.org/10.1111/j.1439-0469.2009.00527.x
  75. Robinson J.A., Ortega-Del Vecchyo D., Fan Z., Kim B.Y., vonHoldt B.M., et al., 2016. Genomic flatlining in the endangered island fox // Curr. Biol. V. 26. P. 1183–1189. https://doi.org/10.1016/j.cub.2016.02.062
  76. Roemer G.W., Smith D.A., Garcelon D.K., Wayne R.K., 2001. The behavioural ecology of the island fox (Urocyon littoralis) // J. Zool. V. 255. № 1. P. 1–14. https://doi.org/10.1017/S0952836901001066
  77. Royauté R., Hedrick A., Dochtermann N.A., 2020. Behavioural syndromes shape evolutionary trajectories via conserved genetic architecture // Proc. R. Soc. B. V. 287. https://doi.org/10.1098/rspb.2020.0183
  78. Schmidt K.A., Dall S.R.X., Gils J.S., van, 2010. The ecology of information: An overview on the ecological significance of making informed decisions // Oikos. V. 119. P. 304–316. https://doi.org/10.1111/j.1600-0706.2009.17573.x
  79. Slobodchikoff C.N. (ed.), 1988. The Ecology of Social Behavior. N.-Y.: Academic Press. 429 p.
  80. Stamps J.A., Buechner M., 1985. The territorial defense hypothesis and the ecology of insular vertebrates // Quart. Rev. Biol. V. 60. P.155–181.
  81. Strand O., Landa A., Linnell J.D.C., Zimmermann B., Skogland T., 2000. Social organization and parental behavior in the arctic fox // J. Mammal. V. 81. № 1. P. 223–233.
  82. Tannerfeldt M., Angerbjörn A., 1996. Life history strategies in a fluctuating environment: Establishment and reproductive success in the arctic fox // Ecography. V. 19. № 3. P. 209–220.
  83. Tarroux A., Berteaux D., Bety J., 2010. Northern nomads: Ability for extensive movements in adult arctic foxes // Polar Biol. V. 33. № 8. P. 1021–1026. https://doi.org/10.1007/s00300-010-0780-5
  84. Trochet A., Courtois E.A., Stevens V.M., Baguette M., Chaine A., et al., 2016. Evolution of sex-biased dispersal // Quart. Rev. Biol. V. 91. № 3. P. 297–330. https://doi.org/10.1086/688097
  85. Wayne R.K., George S.B., Gilbert D., Collins P.W., Kovach S.D., et al., 1991. A morphologic and genetic study of the Island Fox, Urocyon littoralis // Evolution. V. 45. P. 1849–1868. https://doi.org/10.1111/j.1558-5646.1991.tb02692.x
  86. Wey T.W., Spiegel O., Montiglio P.-O., Mabry K.E., 2015. Natal dispersal in a social landscape: Considering individual behavioral phenotypes and social environment in dispersal ecology // Curr. Zool. V. 61. № 3. P. 543–556.
  87. White P.A., 1992. Social Organization and Activity Patterns of the Artic Fox (Alopex lagopus pribilofensis) on St. Paul Island, Alaska. MS Thesis. Berkeley: Univ. of California. 278 p.
  88. Whittaker R.J., Férnandez-Palacios J.M., Matthews T.J., Borregaard M.K., Triantis K.A., 2017. Island biogeography: Taking the long view of nature’s laboratories // Science. V. 357. № 6354. https://doi.org/10.1126/science.aam8326
  89. Wright N., Steadman D.W., Witt C.C., 2016. Predictable evolution toward flightlessness in volant island birds // PNAS. V. 113. № 17. P. 4765–4770. https://doi.org/10.1073/pnas.1522931113

Copyright (c) 2023 М.Е. Гольцман, Е.П. Крученкова, Л.О. Доронина

This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies