Irreversible microevolutionary changes in genotypic composition of sika deer Cervus nippon populations in response to vegetation degradation and food shortage

• Autorzy: Sheremetev I. , Sheremeteva I.
• Języki publikacji: EN

Abstrakty

EN

The present study deals with changes in important skull characteristics of the sika deer Cervus nippon Temminck, 1838 in response to changes in food supply. Moderate food shortage results mainly in a linear reduction in skull size, while severe food shortage results in changes in skull shape. In the deer that returned to habitats with sufficient food supply, some skull parameters recovered to, or even exceeded, normal values, whereas other parameters remained stressed resulting in retention or enhancement of skull distortions. Differences in skull parameters among the populations studied were comparable to those between some cervid species, eg, the Siberian roe deer Capreolus pigargus Pallas, 1771 and European roe deer Capreolus capreolus Linnaeus, 1758 and other deer subspecies. In the introduced sika deer populations, skull distortions were apparently caused by interspecific hybridization. Descendants of the escaped deer have not reverted to the normal phenotype, even over several generations, providing a recent case of true evolutionary changes. This occurred by a change in the ratio of different morphotypical groups, probably due to their different responses to food shortage. Thus sufficient food supply may account for changes in a population’s genotypic composition through selection of characteristics that favour passing on genetic material when food is limited.

Słowa kluczowe

EN

microevolutionary change; genotypic composition; sika deer; Cervus nippon; animal population; vegetation degradation; food shortage; cervid; skull; skull parameter; morphology; craniometrical analysis; starvation; hybridization; food supply

• Wydawca: -
• Czasopismo: Acta Theriologica
• Rocznik: 2010
• Tom: 55
• Numer: 1
• Opis fizyczny: p.9-26,fig.,ref.

Twórcy

autor

Sheremetev I.

• Institute of Biology and Soil Science, FEB of Russian Academy of Science, prospekt 100-letya 159, 690022 Vladivostok, Russia

autor

Sheremeteva I.

Bibliografia

• Abernethy K. 1994. The establishment of a hybrid zone between red and sika deer (genus Cervus). Molecular Ecology 3: 551–562. doi: 10.1111/j.1365-294X.1994.tb00086.x
• Aragon S., Braza F., San Jose C. and Fandos P. 1998. Variation in skull morphology of roe deer (Capreolus capreolus) in western and central Europe. Journal of Mammalogy 79: 131–140. doi: 10.2307/1382847
• Bartos L., Hyanek J. and Zirovnicky J. 1981 Hybridization between red and sika deer: I. craniological analysis. Zoologischer Anzeiger 207: 260–270.
• Bartos L. and Zirovnicky J. 1981. Hybridization between red and sika deer: II. phenotype analysis. Zoologischer Anzeiger 207: 271–287.
• Baryshnikov G. F., Puzachenko A. Yu. and Abramov A. V. 2003. New analysis of variability of check teeth in Eurasian badgers (Carnivora, Mustelidae, Meles). Russian Journal of Theriology 1: 133–149.
• Boeskorov G. G. and Puzachenko A. Yu. 2001. Geographical variability of skull and horns in holarctic moose (Alces, Arthiodactyla). Zoologicheskii Zhurnal 80: 97–110. [In Russian with English summary]
• Bogachev A. S. 1993. [Ecological and morphological studies of sika deer population]. [Science to Far Eastern stockbreeder]. Primorskii Selsko-Khozyaistvennyi Institut, Ussuriisk: 74–78. [In Russian]
• Bradshaw R. H. W., Hannon G. E. and Lister A. M. 2003. A long-term perspective on ungulate-vegetation interactions. Forest Ecology and Management 181: 267–280.
• Bromley G. F. 1984. [Artiodactyls]. [In: Terrestrial mammals of Far East of USSR. V. G. Krivosheev, ed]. Nauka, Moscow: 317–352. [In Russian]
• Bromley G. F. and Kucherenko S. P. 1983. [Artiodactyls of the South Far East of USSR]. Nauka, Moscow: 1–305. [In Russian]
• Carter J., Ackleh A. S., Leonard B. P. and Wang H. B. 1999. Giant panda (Ailuropoda melanoleuca) population dynamics and bamboo (subfamily Bambusoideae) life history: a structured population approach to examining carrying capacity when the prey are semelparous. Ecological Modeling 123: 207–223. doi: 10.1016/S0304-3800 (99)00145-3
• Cattell R. B. 1966. The scree test for the number of factors. Multivariate Behavioral Research 1: 245–276. doi: 10. 1207/s15327906mbr0102_10
• Cavallini P. 1995. Variation in the body size of the red fox. Annales Zoologici Fennici 32: 421–427.
• Croitor R., Bonifay M. F. and Brugal J. P. 2008. Systematic revision of the endemic deer (Haploidoceros) n. gen. (mediterraneus) (BONIFAY, 1967) (Mammalia, Cervidae) from the Middle Pleistocene of Southern France. Palaeontologische Zeitschrift 82: 325–346.
• Danilkin A. A. 1999. [Deer (Cervidae)]. GEOS, Moscow: 1–552. [In Russian]
• East R. 1984. Rainfall, soil nutrient status and biomass of large African savanna mammals. African Journal of Ecology 22: 245–270. doi: 10.1111/j.1365-2028.1984. tb00700.x
• Estevez J. A., Landete-Castillejos T., Martínez A., García A. J., Ceacero F., Gaspar-López E., Calatayud A. and Gallego L. 2009. Antler mineral composition of Iberian red deer Cervus elaphus hispanicus is related to mineral profile of diet. Acta Theriologica 54: 235–242. doi: 10.4098/ j.at.0001-7051.070.2008
• Evin A., Baylac M., Ruedi M., Mucedda M. and Pons J. M. 2008. Taxonomy, skull diversity and evolution in a species complex of Myotis (Chiroptera: Vespertilionidae): a geometric morphometric appraisal. Biological Journal of the Linnean Society 95: 529–538.
• Fernandez M. H., Sierra M. A. A. and Pelaez-Campomanes P. 2007. Bioclimatic analysis of rodent palaeofaunas reveals severe climatic changes in Southwestern Europe during the Plio-Pleistocene. Palaeogeography Palaeoclimatology Palaeoecology 251: 500–526.
• Frankham R. 1995. Inbreeding and extinction — a threshold effect. Conservation biology 9: 792–799. doi: 10.1046/ j.1523-1739.1995.09040792.x
• Grant P. R. and Grant B. R. 1995. Predicting microevolutionary responses. Evolution 49: 241–251. doi: 10.2307/ 2410334
• Goodman S. J., Barton N. H., Swanson G., Abernethy K. and Pemberton J. M. 1999. Introgression through rare hybridization: A genetic study of a hybrid zone between red and sika deer (genus Cervus) in Argyll, Scotland. Genetics 152: 355–371.
• Hartley S. E. and Jones T. H. 2003. Plant diversity and insect herbivores: effects of environmental change in contrasting model systems. Oikos 101: 6–17. doi: 10.1034/j. 1600-0706.2003.12566.x
• Hayward M. W. 2009. Conservation management for the past, present and future. Biodiversity and Conservation 18: 765–775. doi:10.1007/s10531-008-9436-y
• Hayward M. W., O’Brien J. and Kerley G. I. H. 2007. Carrying capacity of large African predators: predictions and tests. Biological Conservation 139: 219–229. doi: 10. 1016/j.biocon.2007.06.018
• Hofmann R. R., Saber A. S., Pielowski Z. and Fruziński B. 1988. Comparative morhological investigations of forest and field ecotypes of roe deer in Poland. Acta Theriologica 33: 103–114.
• Holodova M. V., Mescherskii I. G., Vorobjov P. A., Pischulina S. L. and Sorokin P. A. 2008. A gene pool dynamics of rare and important game species of mammals in Russia. [In: Biodiversity and gene pool dynamics. I. A. Zaharov-Gezehus, ed]. Proceedings of Symposia: 121–122.
• James F. C. and McCulloch C. E. 1990. Multivariate analysis in ecology and systematics: panacea or Pandora’s box? Annual Review of Ecology and Systematics 21: 129–166. doi: 10.1146/annurev.es.21.110190.001021
• Jędrzejewska B., Okarma H., Jędrzejewski W. and Miłkowski L. 1994. Effects of exploitation and protection on forest structure, ungulate density and wolf predation in Białowieża Primeval Forest, Poland. Journal of Applied Ecology 31: 664–676. doi: 10.2307/2404157
• Jefferies R. L., Klein D. R. and Shaver G. R. 1994. Vertebrate herbivores and northern plant communities — recoprocal influences and responses. Oikos 71: 193–206. doi: 10.2307/3546267
• Jiang Z. W., Hamasaki S., Ueda H., Kitahara M. and Takatsuki S. 2006. Sexual variations in food quality and gastrointestinal features of sika deer (Cervus nippon) in Japan during winter: Implications for feeding strategy. Ecological Research 7: 19–23. doi: 10.2108/zsj.23.543
• Kalinina V. N. and Solovjev V. I. 2003. [The introduction in multivariate techniques]. GUU, Moscow: 1–66. [In Russian]
• Kie J. G. and Lehmkuhl J. F. 2001. Herbivory by wild and domestic ungulates in the intermountain west. Northwest Science 75: 55–61.
• Kruskal J. B. 1986. [Multidimensional scaling and others techniques of structure analysis]. [In: Statistical procedures for computers. M. B. Maljutov, ed]. Nauka, Moscow: 301–347. [In Russian]
• Kupriyanova I. F., Puzachenko A. Yu. and Agajanyan A. K. 2003. Temporal and spatial variability of the skulls of the common shrew Sorex araneus (Insectivora). Zoologicheskii Zhurnal 82: 839–851. [In Russian]
• Kurt F., Hartl G. B. and Volk F. 1993. Breeding strategies and genetic-variation in European roe deer Capreolus capreolus populations. Acta Theriologica 38, Suppl.: 187–194.
• Li C. C. 1955. Population genetic. University Chicago Press, Chicago: 1–346.
• Loehr J., Kovanen M., Carey J., Högmander H., Jurasz C., Kärkkäinen S., Suhonen S. and Ylönen H. 2005. Gender-and age-class-specific reactions to human disturbance in a sexually dimorphic ungulate. Canadian Journal of Zoology 83: 1602–1607. doi: 10.1139/z05-162
• Lowe V. P. W. and Gardiner A. S. 1975. Hybridization between red deer (Cervus elaphus) and sika deer (Cervus nippon) with particular reference to stocks in N.W. England. Journal of Zoology, London 177: 553–566. doi: 10.1111/j.1469-7998.1975.tb02259.x
• Lu X. P., Wei F. W., Li M., Yang G. and Liu H. 2006. Genetic diversity among Chinese sika deer (Cervus nippon) populations and relationships between Chinese and Japanese sika deer. Chinese Science Bulletin 51: 433–440. doi: 10.1007/s11434-006-0433-9
• Ludt C. J., Schroeder W., Rottmann O. and Kuehn R. 2004. Mitochondrial DNA phylogeography of red deer (Cervus elaphus). Molecular Phylogenetics and Evolution 31: 1064–1083. doi: 10.1016/j.ympev.2003.10.003
• Makovkin L. I. 1999. Wild sika deer of Lasovskii Reserve and adjacent area. Russkii Ostrov Press, Vladivostok: 1–133. [In Russian with English summary]
• Marean C. W. and Gifford-Gonzalez D. 1991. Late Quarternary extinct ungulates of East Africa and paleoenvironmental implications. Nature 350: 418–420. doi: 10. 1038/350418a0
• Miroljubov I. I. and Rjaschenko L. P. 1948. [Sika deer]. DZT Press, Vladivostok: 1–116. [In Russian]
• Moe B., Brunvoll S., Mork D., Brobakk T. E. and Bech C. 2004. Developmental plasticity of physiology and morphology in diet-restricted European shag nestlings (Phalacrocorax aristotelis). Journal of Experimental Biology 207: 4067–4076. doi: 10.1242/jeb.01226
• Morellet N., Gaillard J. M., Hewison A. J. M., Ballon P., Boscardin Y., Duncan P., Klein F. and Maillard D. 2007. Indicators of ecological change: new tools for managing populations of large herbivores. Journal of Applied Ecology 44: 634–643. doi: 10.1111/j.1365-2664.2007.01307.x
• Mueller T., Olson K. A., Fuller T. K., Schaller G. B., Murray M. G. and Leimgruber P. 2008. In search of forage: predicting dynamic habitats of Mongolian gazelles using satellite-based estimates of vegetation productivity. Journal of Applied Ecology 45: 649–658. doi: 10.1111/j. 1365-2664.2007.01371.x
• Nesterenko V. A., Sheremetyev I. S. and Alexeeva E. V. 2002. Dynamics of the shrew taxocene structure in the Late Quaternary of the southern Far East. Paleontologicheskii Zhurnal 5: 93–99.
• Ozaki M., Suwa G., Kaji K., Ohba T., Hosoi E., Koizumi T. and Takatsuki S. 2007. Correlations between feeding type and mandibular morphology in the sika deer. Journal of Zoology, London 272: 244–257. doi: 10.1111/j.1469-7998.2006.00264.x
• Palombo M. R., Sardella R. and Novelli M. 2008. Carnivora dispersal in Western Mediterranean during the last 2.6Ma. Quarternary International 179: 176–189. doi: 10.1016/j.quaint.2007.08.029
• Pavlinov I. Y. 2003. [Systematics of recent mammals]. Moscow University Publisher, Moscow: 1–297. [In Russian]
• Pianka E. R. 1981. [Evolutionary ecology]. Mir, Moscow: 1–400. [In Russian]
• Potapova E. G. 2000. Pathways of transforming mandible morphology in Dipodoidea (Rodentia) and the role of various adaptations in their specific features. Zoologicheskii Zhurnal 79: 1445–1456. [In Russian with English summary]
• Preen A. and Marsh H. 1995. Response of dugongs to largescale loss of seagrass from Hervey bay, Queensland, Australia. Wildlife Research 22: 507–519. doi: 10.1071/ WR9950507
• Prisiajnuk N. P. and Prisiajnuk V. E. 1974. [Forage plants of the sika deer through taxa, life modes, and seasons]. [In: Sika deer in South Primorie. Y. N. Chichikin, ed]. Kyrgizstan, Frunze: 3–61. [In Russian]
• Prisiajnuk V. E. 1981. Morphometric characteristics of the indigenous sika deer (Cervus nippon hortulorum) from Primorie. Zoologicheskii Zhurnal 60: 1817–1828. [In Russian with English summary]
• Puzachenko A. Yu. 2001. Skull variability in the common mole rat Spalax microphtalmus (Spalacidae, Rodentia). 1. A method for analysis of data, nonage variability in males. Zoologicheskii Zhurnal 80: 343–357. [In Russian with English summary]
• Puzachenko Yu. G. 2004. [Mathematical techniques in ecological and geographical researches]. Akademiya, Moscow: 1–416. [In Russian]
• Puzachenko A. Yu. 2006. Variability of skull in lesser mole rats of the genus Nannospalax (Spalacidae, Rodentia). Zoologicheskii zhurnal 80: 343–357. [In Russian with English summary]
• Saccheri I., Kuussaari M., Kankare M., Vikman P., Fortelius W. and Hanski I. 1998. Inbreeding and extinction in a butterfly metapopulation. Nature 392: 491–494.
• Schaefer J. A., Bergman C. M. and Luttich S. N. 2000. Site fidelity of female caribou at multiple spatial scales. Landscape Ecology 15: 731–739.
• Senn H. V. and Pemberton J. M. 2009. Variable extent of hybridization between invasive sika (Cervus nippon) and native red deer (C. elaphus) in a small geographical area. Molecular ecology 18: 862–876. doi: 10.1111/j. 1365-294X.2008.04051.x
• Sheremetyev I. S. and Prokopenko S. V. 2005. Feeding ecology of Far Eastern ungulates. Dalnauka, Vladivostok: 1–167. [In Russian with English summary]
• Sheremetyev I. S. and Prokopenko S. V. 2006. General analysis of forest vegetation in the south of the Far East with regard to the feeding of wild ruminants (Artiodactyla, Ruminantia). Russian Journal of Ecology 37: 217–224. doi: 10.1134/S1067413606040011
• Sheremetyev I. S., Salkina G. P. and Bogachev A. S. 2004 Variation of craniometric characteristics of the Ussurian sika Cervus nippon hortulorum (Artiodactyla, Cervidae) from Primorie. Zoologicheskii Zhurnal 83: 1499–1507. [In Russian with English summary]
• Sheremetyeva I. N. 2007. Geographical variation of craniological parameters in the reed vole Microtus fortis (Rodentia, Cricetidae). Zoologicheskii Zhurnal 86: 751–760. [In Russian with English summary]
• Sheremetyeva I. N., Kartavtseva I. V., Voyta L. L., Kryukov A. P. and Haring E. 2009. Morphometric analysis of intraspecific variation in Microtus maximowiczii (Rodentia, Cricetidae) in relation to chromosomal differentiation with reinstatement of Microtus gromovi Vorontsov, Boeskorov, Lyapunova et Revin, 1988, stat. nov. Journal of Zoological Systematics and Evolutionary Research 47: 42–48. doi: 10.1111/j.1439-0469.2008.00511.x
• Sheremetyeva I. N. and Sheremetyev I. S. 2008. Skull variation in the Siberian roe deer Capreolus pygargus from the Far East: A revision of the distribution of the subspecies. European Journal of Wildlife Research 54: 557–569. doi: 10.1007/s10344-008-0180-0
• Sherman P. W. and Runge M. C. 2002. Demography of a population collapse: The Northern Idaho ground squirrel (Spermophilus brunneus brunneus). Ecology 83: 2816–2831. doi: 10.1890/0012-9658(2002)083[2816: DOAPCT] 2.0.CO,2 Shrestha R. and Wegge P. 2008. Wild sheep and livestock in Nepal Trans-Himalaya: coexistence or competition? Environmental Conservation 35: 125-136. doi: 10.1017/ S0376892908004724
• Sinclair A. R. E., Mduma S. A. R., Hopcraft J. G. C., Fryxell J. M., Hilborn R. and Thirgood S. 2007. Long-term ecosystem dynamics in the Serengeti: Lessons for conservation. Conservation Biology 21: 580–590. doi: 10.1111/j.1523-1739.2007.00699.x
• Statistica 8. 2007. Statistica for Windows, version 8.0. StatSoft, Inc.
• Steklenev E. P. 1986. [Interspecific hybridization between red (Cervus elaphus L.) and sika deer (Cervus nippon hortulorum Temm.)]. Russian Journal of Cytology and Genetics 20: 138–142. [In Russian]
• Takatsuki S. 1992. Foot morphology and distribution of sika-deer in relation to snow depth in Japan. Ecological Research 7: 19–23. doi: 10.1007/BF02348593
• Van Tongeren O., Gremmen N. and Hennekens S. 2008. Assignment of releves to pre-defined classes by supervised clustering of plant communities using a new composite index. Journal of Vegetation Science 19: 525–536.
• Vavra M., Parks C. G. and Wisdom M. J. 2007. Biodiversity, exotic plant species, and herbivory: The good, the bad, and the ungulate. Forest Ecology and Management 246: 66–72. doi: 10.1016/j.foreco.2007.03.051
• Vistnes I. I. and Nellemann C. 2008. Reindeer winter grazing in alpine tundra: impacts on ridge community composition in Norway. Arctic Antarctic and Alpine Researches 40: 215–224.
• Williams U. T. and Lans J. N. 1986. [Methods of hierarchical classification]. [In: Statistical procedures for computers. M. B. Maljutov, ed]. Nauka, Moscow: 269–301. [In Russian]
• Young T. P. 1994. Natural die-offs of large mammals — implications for conservation. Conservation Biology 8: 410–418. doi: 10.1046/j.1523-1739.1994.08020410.x
• Yuasa T., Nagata J., Hamasaki S., Tsuruga H. and Furubayashi K. 2007. The impact of habitat fragmentation on genetic structure of the Japanese sika deer (Cervus nippon) in southern Kantoh, revealed by mitochondrial D-loop sequences. Ecological Research 22: 97–106. doi: 10.1007/s11284-006-0190-x