The effects of coccidian infection and predators on reproductive performance of root vole (Alexandromys oeconomus)

doi:10.16829/j.slxb.150547

Abstract

Abstract: In nature, predators and parasites are two major extrinsic population regulators, their interaction can play important roles on the prey/host population dynamics. However, some studies found that coccidia with lower infection intensity and predators have no significant interactive effects on the reproduction of root voles (Alexandromys oeconomus). In the wild, coccidian infection in root voles has seasonal variation, and their infection peak of prevalence and intensity occur in autumn. Whether the primary effect of coccidian infection or the interactive effects of coccidian infection and predators can affect the reproduction of root voles are obscure. To test the main and interactive effects of coccidian infection with higher intensity and predators on reproduction of root voles, the two-level factorial design was conducted. Then, the prevalence and intensity of intestinal parasites, testicular index, testosterone levels, sperm density, sperm motility and ovary index were evaluated. Our results showed that coccidian infection with higher intensity significantly suppressed the reproductive performance of voles, but had no significant difference in the interaction between coccidian infection and predators, which may correlate with the time mismatch. We suggested that coccidian infection had a slightly limited effect on the reproduction of small mammal populations, but they could affect the fluctuation of host populations via reducing the overwinter survival of the host when interacted with predators.

Key words: Coccidian infection, Predation, Reproductive performance, Root vole (Alexandromys oeconomus)

摘要： 在自然界，捕食者和寄生物是两种主要的种群外部调节因子，二者的交互作用会对猎物和宿主种群波动产生深远影响。较低的球虫感染强度与捕食对根田鼠（Alexandromys oeconomus）繁殖无显著的交互作用。自然界球虫感染存在季节性变化，秋季感染强度最高。为了探究较高感染强度下，球虫与捕食对根田鼠繁殖的主效应及交互作用，本研究采用2×2析因实验设计，在野外围栏中测定了根田鼠种群肠道内寄生物的感染率和感染强度、雄性睾丸指数、睾酮水平、精子密度、精子活力以及雌性卵巢指数。结果表明，较高的感染强度下，球虫能显著抑制根田鼠的繁殖性能，但球虫感染与捕食对根田鼠的繁殖无显著的交互作用，这可能与球虫感染和捕食效应在时间上的错配有关。本研究认为，球虫感染对繁殖期小哺乳动物种群的调节作用虽有限，但其可通过与捕食者的耦合来降低宿主越冬时的存活率，进而影响宿主种群波动。

关键词: 球虫感染, 捕食, 繁殖性能, 根田鼠

CLC Number:

Q494

YANG Yuangang, SHANG Guozhen, BIAN Jianghui. The effects of coccidian infection and predators on reproductive performance of root vole (Alexandromys oeconomus)[J]. ACTA THERIOLOGICA SINICA, 2021, 41(6): 676-684.

杨元罡, 尚国珍, 边疆晖. 球虫感染与捕食对根田鼠繁殖性能的影响[J]. 兽类学报, 2021, 41(6): 676-684.

References

Anderson R M, May R M. 1978. Regulation and stability of host-parasite population interactions:I. Regulatory processes. Journal of Animal Ecology, 47:219-247.
Alzaga V, Vicente J, Villanua D, Acevedo P, Casas F, Gortazar C. 2008. Body condition and parasite intensity correlates with escape capacity in Iberian hares (Lepus granatensis). Behavioral Ecology and Sociobiology, 62 (5):769-775.
Ahad S, Tanveer S, Malik T A. 2015. Seasonal impact on the prevalence of coccidian infection in broiler chicks across poultry farms in the Kashmir valley. Journal of Parasitic Diseases, 39 (4):736-740.
Bush A O, Lafferty K D, Lotz J M, Shostak A W. 1997. Parasitology meets ecology on its own terms:Margolis et al. revisited. The Journal of Parasitology, 83 (4):575-583.
Boonstra R, Krebs C J, Stenseth N C. 1998. Population cycles in small mammals:the problem of explaining the low phase. Ecology, 79 (5):1479-1488.
Bolker B M, Brooks M E, Clark C J, Geange S W, Poulsen J R, Stevens M H H, White J S. 2009. Generalized linear mixed models:a practical guide for ecology and evolution. Trends in Ecology and Evolution, 24 (3):127-135.
Bian J H, Wu Y, Liu J K. 2005. Breeding behavior under temporal risk of predation in male root voles (Microtus oeconomus). Journal of Mammalogy, 86 (5):953-960.
Bian J H, Wu Y, Zhou K K. 2008. Effect of population density on demography and individual corticosterone level during breeding period in root voles (Microtus oeconomus). Acta Theriologica Sinica, 28 (2):135-143. (in Chinese)
Bian J H, Du S Y, Wu Y, Cao Y F, Nie X H, He H, You Z B. 2015. Maternal effects and population regulation:maternal density-induced reproduction suppression impairs offspring capacity in response to immediate environment in root voles Microtus oeconomus. Journal of Animal Ecology, 84 (2):326-336.
Cao Y F, Nie X H, He H, Du S Y, Donald W D, Bian J H. 2014. Gastrointestinal parasites of root voles, Microtus oeconomus (Rodentia:Muridae) from Haibei area, Qinghai Province, China. Comparative Parasitology, 81 (2):185-190.
Dai J X. 1990. Qinghai-Tibet Plateau Climate. Beijing:China Meteorological Press. (in Chinese)
Du S Y, Cao Y F, Nie X H, Wu Y, Bian J H. 2016. The synergistic effect of density stress during the maternal period and adulthood on immune traits of root vole (Microtus oeconomus) individuals-a field experiment. Oecologia, 181 (2):335-346.
Elton C S. 1942. Voles, Mice and Lemmings. Oxford:Oxford University Press.
Faccio L, Silva A S D, Tonin A A, Oberherr L, Gressler L T, Oliveira D T, Sangoi M B, Moresco R N, Samara Y N, Veiga M, Duarte M M M F, Monteiro S G. 2014. Relationship between testicular lesion and hormone levels in male rats infected with Trypanosoma evansi. Anais Da Academia Brasileira De Ciências, 86 (3):1537-1546.
Gooderham K, Schulte-Hostedde A. 2011. Macroparasitism influences reproductive success in red squirrels (Tamiasciurus hudsonicus). Behavioral Ecology, 22 (6):1195-1200.
Heikkilä J, Kaarsalo K, Mustonen O, Pekkarinen P. 1993. Influence of predation risk on early development and maturation in three species of Clethrionomys voles. Annales Zoologici Fennici, 30(2):153-161.
Hakkarainen H, Huhta E, Koskela E, Mappes T, Soveri T, Suorsa P. 2006. Eimeria-parasites are associated with a lowered mother's and offspring's body condition in island and mainland populations of the bank vole. Parasitology, 134 (1):23-31.
Jędrzejewski W, Rychlik L, Jędrzejewska B. 1993. Responses of bank voles to odours of seven species of predators:experimental data and their relevance to natural predator-vole relationships. Oikos, 68:251-257.
Jiang Y J, Wei S W, Wang Z W, Cui R X, Sun R Y. 1991. Productivity investigation of the root vole (Microtus oeconomus) population in the Haibei alpine bushland (Potentilla fruticosa) Ⅰ. Population dynamics. Acta Theriologica Sinica, 11 (4):270-278. (in Chinese)
Liang J R, Zeng J X, Wang Z W, Han Y C. 1982. Studies on growth and development in the root vole (Microtus oeconomus). In:Xia W P ed. Acta Biologica Plateau Sinca. Beijing:Science Press, 1:19-20. (in Chinese)
Liu J K, Liang J R, Zhou X M, Li J H. 1982. The rodents community and quantity in Alpine Meadow Ecosystem Research Station. In:Xia W P ed. Alpine Meadow Ecosystem. Lanzhou:Gansu People's Publishing House, 1:34-43. (in Chinese)
Liu J K, Su J P, Liu W, Wang X, Nie H Y, Li Y M. 1994. Field experimental studies on the multifactorial hypothesis of population system regulation for small rodents:an analysis of effects of food availability and predation on population dynamics of root vole. Acta Theriologica Sinica, 14 (2):117-129. (in Chinese)
Laakkonen J, Oksanen A, Soveri T, Henttonen H. 1998. Dynamics of intestinal coccidia in peak density Microtus agrestis, Microtus oeconomus and Clethrionomus glareolus populations in Finland. Ecography, 21:135-139.
Li Y N, Zhao X Q, Cao G M, Zhao L, Wang Q X. 2004. Analyses on climates and vegetation productivity background at Haibei Alpine Meadow Ecosystem Research Station. Plateau Meteorology, 23(4):558-567. (in Chinese)
Lassen B, Viltrop A, Järvis T. 2009. Herd factors influencing oocyst production of Eimeria and Cryptosporidiumin Estonian dairy cattle. Parasitology Research, 105 (5):1211-1222.
May R M, Anderson R M. 1979. Population biology of infectious diseases:Part II. Nature, 280:455-461.
Mazurkiewicz M. 1991. Population dynamics and demography of the bank vole in different tree stands. Acta Theriologica, 36:207-227.
Merkens M, Harestad A S, Sullivan T P. 1991. Cover and efficacy of predator-based repellents for Townsend's vole. Journal of Chemical Ecology, 17:401-412.
Marino Jr J A, Werner E E. 2013. Synergistic effects of predators and trematode parasites on larval green frog (Rana clamitans) survival. Ecology, 94 (12):2697-2708.
Norrdahl K, Korpimäki E. 1995. Mortality factors in a cyclic vole population. Proceedings of the Royal Society B-Biological Sciences, 261 (1360):49-53.
Neuhaus P. 2003. Parasite removal and its impact on litter size and body condition in Columbian ground squirrels (Spermophilus columbianus). Proceedings of the Royal Society B:Biological Sciences, 270 (Suppl 2):S213-S215.
Newey S, Thirgood S J, Hudson P J. 2004. Do parasite burdens in spring influence condition and fecundity of female mountain hares Lepus timidus? Wildlife Biology, 10 (3):171-176.
Nie X H, Cao Y F, Du S Y, He H, Bian J H. 2014. Intestinal parasites prevalence in root voles (Microtus oeconomus) from field enclosures. Acta Theriologica Sinica, 34 (2):172-180. (in Chinese)
Ocaido M, Siefert L, Baranga J. 1999. Seasonal changes of impala(Aepyceros melampus, Lichtenstein, 1812) faecal helminth egg counts through a one-year period. African Journal of Ecology, 37(3):327-333.
Steen H. 1995. Untangling the causes of disappearance from a local population of root voles, Microtus oeconomus:a test of the regional synchrony hypothesis. Oikos, 73 (1):65-72.
Steen H, Taitt M, Krebs C J. 2002. Risk of parasite-induced predation:an experimental field study on Townsend's voles (Microtus townsendii). Canadian Journal of Zoology, 80 (7):1286-1292.
Schabenberger O. 2005. Introducing the GLMMIX procedure for generalized linear mixed models. SUGI Proceedings, 30:196-300.
Pyziel A M, Demiaszkiewicz A W. 2015. Observations on sporulation of Eimeria bovis (Apicomplexa:Eimeriidae) from the European bison Bison bonasus:effect of temperature and potassium dichromate solution. Folia Parasitologica, 62:020.
Schai-Braun S C, Posautz A, Alves P C, Hacklaender K. 2019. Gastrointestinal parasite infestation in the alpine mountain hare (Lepus timidus varronis):are abiotic environmental factors such as elevation, temperature and precipitation affecting prevalence of parasite species? International Journal for Parasitology-Parasites and Wildlife, 9:202-208.
Shang G Z, Zhu Y H, Wu Y, Cao Y F, Bian J H. 2019. Synergistic effects of predation and parasites on the overwinter survival of root voles. Oecologia, 191 (1):83-96.
Shang G Z, Yang Y G, Zhu Y H, Wu X Q, Cao Y F, Wu Y, Bian J H. 2020. A complex regulating pattern induced by the effects of predation and parasites on root vole (Microtus oeconomus) populations during the breeding season. Journal of Mammalogy, 101(5):1345-1355.
Tompkins D M, Dunn A M, Smith M J, Telfer S. 2011. Wildlife diseases:from individuals to ecosystems. Journal of Animal Ecology, 80:19-38.
Wetzel R. 1951. Verbesserte Mcmaster-Kammer zum Auszählen von Wurmeiern. Tierärztl Umsch, 6:209-210.
Werner E E, Peacor S D. 2003. A review of trait-mediated indirect interactions in ecological communities. Ecology, 84 (5):1083-1100.
Wascher C A F, Bauer A C, Holtmann A R, Kotrschal K. 2012. Environmental and social factors affecting the excretion of intestinal parasite eggs in graylag geese. Behavioral Ecology, 23 (6):1276-1283.
Yang F T. 1982. The natural profile in Alpine Meadow Ecosystem Research Station. In:Xia W P ed. Alpine Meadow Ecosystem. Lanzhou:Gansu People's Publishing House, 1:1-8. (in Chinese)
Yang L, Wu Y, Cao Y F, Chen F, Bian J H, Chen Z. 2011. Effect of maternal density in field enclosures on sex organ index of F1 offspring in root voles (Microtus oeconomus). Acta Theriologica Sinica, 31 (2):164-170. (in Chinese)
Yang Y B, Shang G Z, Du S Y, Zhang X, Wu Y, Bian J H. 2018. Maternal density stress and coccidian parasitism:synergistic effects on overwinter survival in root voles. Functional Ecology, 32 (9):2181-2193.
Yin B F, Wang J L, Wei W H, Zhang Y M, Cao Y F. 2004. Population reproductive characteristics of plateau pika in alpine meadow ecosystem. Acta Theriologica Sinica, 24 (3):222-228. (in Chinese).
Yin B F, Yang S M, Shang G Z, Wei W H. 2017. Effects of predation risk on behavior, hormone levels, and reproductive success of plateau pikas. Ecosphere, 8:e01643.
Zhu Y H, Shang G Z, Yang Y B, Zhang X, Wu Y, Cao Y F, Bian J H. 2018. The susceptibility of intestinal parasites induced by predation risk to over-wintering root voles (Microtus oeconomus). Acta Theriologica Sinica, 38 (5):467-476. (in Chinese)
边疆晖, 吴雁, 周抗抗. 2008.繁殖期根田鼠种群密度对其种群统计参数及个体皮质酮水平的作用.兽类学报, 28 (2):135-143.
刘季科, 梁杰荣, 周兴民, 李健华. 1982.高寒草甸生态系统定位站的啮齿动物群落与数量.见:夏武平主编.高寒草甸生态系统.兰州:甘肃人民出版社, 1:34-43.
刘季科, 苏建平, 刘伟, 王溪, 聂海燕, 李玉敏. 1994.小型啮齿动物种群系统调节复合因子理论的野外实验研究:食物可利用性和捕食对根田鼠种群动态作用的分析.兽类学报, 14 (2):117-129.
朱亚辉, 尚国珍, 杨彦宾, 张鑫, 吴雁, 曹伊凡, 边疆晖. 2018.捕食风险对根田鼠越冬肠道寄生物易感性的影响.兽类学报, 38 (5):467-476.
李英年, 赵新全, 曹广民, 赵亮, 王勤学. 2004.海北高寒草甸生态系统定位站气候, 植被生产力背景的分析.高原气象, 23 (4):558-567.
杨福囤. 1982.青海高寒草甸生态系统定位站的自然地理概况.见:夏武平主编.高寒草甸生态系统.兰州:甘肃人民出版社, 1:1-8.
杨乐, 吴雁, 曹伊凡, 陈芳, 边疆晖, 陈志. 2011.围栏条件下母体密度应激对根田鼠 F1代性器官指数的影响.兽类学报, 31 (2):164-170.
姜永进, 魏善武, 王祖望, 郑生武, 崔瑞贤, 孙儒泳. 1991.海北高寒草甸金露梅灌丛根田鼠种群生产力的研究Ⅰ.种群动态.兽类学报, 11 (4):270-278.
殷宝法, 王金龙, 魏万红, 张堰铭, 曹伊凡. 2004.高寒草甸生态系统中高原鼠兔的繁殖特征.兽类学报, 24 (3):222-228.
聂绪恒, 曹伊凡, 堵守杨, 何惠, 边疆晖. 2014.野外围栏条件下根田鼠肠道寄生物的感染率.兽类学报, 34 (2):172-180.
梁杰荣, 曾缙祥, 王祖望, 韩永才. 1982.根田鼠生长和发育的研究.见:夏武平主编.高原生物学集刊.北京:科学出版社, 1:19-20.

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