Scatter-Hoarding the Seeds of Sympatric Forest Trees by Apodemus peninsulae in a Temperate Forest in Northeast China

• Autorzy: Li D. , Jin Z. , Yang C. , Yang C. , Zhang M.

Identyfikatory

DOI

10.3161/15052249PJE2018.66.4.006

• Języki publikacji: EN

Abstrakty

EN

As the main predator and disperser of seeds, rodents play an important role in the process of vegetation regeneration by adopting different foraging and hoarding strategies in forest ecosystems. Infrared automated detection cameras and seed-tagging methods were used to understand the effects of rodents on seeds in natural environments. We chose the dominant species Apodemus peninsulae (Korean field mouse) as the focus of this study, and seeds of the three species Pinus koraiensis, Corylus mandshurica and Quercus mongolica were released and tracked in a temperate forest in northeast China. The results showed that approximately 80% of the seeds were manipulated by A. peninsulae, 15.1% of the seeds were used as food, 20.4% of the seeds were handled after feeding, 41.3% of the seeds were handled during storage, and 23.3% of the seeds remained intact. In addition, A. peninsulae preferred Q. mongolica (85.3%) and P. koraiensis (85.6%) over C. mandshurica (59.2%). The rodents frequently hoarded seeds from every species in many small, close-range, widely dispersed, single scatter-hoarded caches around the seed station. Most caches were dispersed approximately 2-4 m from the seed station. The results indicated that A. peninsulae adopted significant discriminatory processing strategies for predation, consumption, dispersal and hoarding of the different seeds of sympatric species. Seed size, proportion of kernel mass, nutrient content, and hull thickness characteristics affected the scatter-hoarding decision processes.

Słowa kluczowe

EN

Apodemus peninsulae; korean mouse; cache size; scatter-hoarding; seed dispersal; seed fate; seed traits

PL

Apodemus peninsulae; myszarka koreańska; wielkość pamięci podręcznej; akwizycja rozproszona; rozproszenie nasion; los nasion; cechy nasion

• Wydawca: Museum and Institute of Zoology, Polish Academy of Sciences
• Czasopismo: Polish Journal of Ecology
• Rocznik: 2018
• Tom: Vol. 66, nr 4
• Strony: 382--394
• Opis fizyczny: Bibliogr. 50 poz., rys., tab., wykr.

Twórcy

autor

Li D.

• College of Wildlife Resource, Northeast Forestry University, Harbin 150040, China
• College of Life Sciences and Technology, Mudanjiang Normal University, Mudanjiang 157011, China

autor

Jin Z.

• College of Wildlife Resource, Northeast Forestry University, Harbin 150040, China
• College of Life Sciences and Technology, Mudanjiang Normal University, Mudanjiang 157011, China

autor

Yang C.

• College of Life Sciences and Technology, Mudanjiang Normal University, Mudanjiang 157011, China

autor

Yang C.

• College of Life Sciences and Technology, Mudanjiang Normal University, Mudanjiang 157011, China

autor

Zhang M.

• College of Wildlife Resource, Northeast Forestry University, Harbin 150040, China

Bibliografia

• [1] Chang G., Xiao Z., Zhang Z. 2010 – Effects of burrow condition and seed handling time on hoarding strategies of Edward's long-tailed rat (Leopoldamys edwardsi) – Behav. Process.85: 163-166.
• [2] Chang G., Zhang Z. 2011 – Differences in hoarding behaviors among six sympatric rodent species on seeds of oil tea (Camellia oleifera) in southwest China – Acta Oecol.37: 165-169.
• [3] Charnov E. L. 1976 – Optimal foraging, the marginal value theorem – Theor. Popul. Biol.9: 129-136.
• [4] Clarke M. F., Kramer D. L. 1994 – Scatter-hoarding by a larder-hoarding rodent: intraspecific variation in the hoarding behaviour of the eastern chipmunk, Tamias striatus – Anim. Behav.48: 299-308.
• [5] Garcia D., Banuelos M. J., Houle G. 2002 – Differential effects of acorn burial and litter cover on Quercus rubra recruitment at the limit of its range in eastern north America – Can. J. Bot.80: 1115-1120.
• [6] Hurly T. A., Lourie S. A. 1997 – Scatter-hoarding and larderhoarding by red squirrels: size, dispersion, and allocation of hoards – J. Mammal.78: 529-537.
• [7] Jacobs L. F. 1992 – The effect of handling time on the decision to cache by grey squirrels – Anim. Behav.43: 522-524.
• [8] Jansen P. A., Visser M. D., Wright S. J., Gemma R., Muller-Landau H. C. 2014 – Negative density dependence of seed dispersal and seedling recruitment in a neotropical palm – Ecol. Lett.17: 1111-1120.
• [9] Janzen D. H. 1971 – Seed predation by animals – Annu. Rev. Ecol. Syst.2: 465-492.
• [10] Jenkins S. H. 2011 – Sex differences in repeatability of food-hoarding behavior of kangaroo rats – Anim. Behav.81: 1155-1162.
• [11] Jenkins S. H., Breck S. W. 1998 – Differences in food hoarding among six species of heteromyid rodents – J. Mammal.79: 1221-1233.
• [12] Jensen T. S. 1985 – Seed-seed predator interactions of European beech, Fagussilvatica and forest rodents, Clethrionomys glareolus and Apodemus flavicollis – Oikos, 44: 149-156.
• [13] Kerley G., Erasmus T. 1991 – What do mice select for in seeds? – Oecologia, 86: 261-267.
• [14] Lai X., Guo C., Xiao Z. 2014 – Trait-mediated seed predation, dispersal and survival among frugivore-dispersed plants in a fragmented subtropical forest, southwest china – Integr. Zool.9: 246-254.
• [15] Li H. J., Zhang Z. B. 2003 – Effect of rodents on acorn dispersal and survival of the liaodong oak (Quercus liaotungensis, Koidz.) – Forest Ecol. Manag.176: 387-396.
• [16] Lichti N. I., Steele M. A., Swihart R. K. 2015 – Seed fate and decision-making processes in scatter-hoarding rodents – Biol. Rev. Camb. Philos. Soc.92: 474.
• [17] Luna C. A., Loayza A. P., Squeo F. A. 2016 – Fruit size determines the role of three scatter-hoarding rodents as dispersers or seed predators of a fleshy-fruited Atacama desert shrub – PLoS ONE, 11: e0166824.
• [18] Lu J., Zhang Z. 2005 – Food hoarding behaviour of large field mouse Apodemus peninsulae – Acta Theriol.50: 51-58.
• [19] Merceron N. R., De Langhe A., Dubois H., Garin O., Gerarts F., Jacquemin F.et al. 2017 – Removal of acorns of the alien oak Quercus rubra on the ground by scatter-hoarding animals in Belgian forests – Biotechnol. Agron. Soc. Environ.21: 127-130.
• [20] Moore J. E., Mceuen A. B., Swihart R. K., Contreras T. A., Steele M. A. 2007 – Determinants of seed removal distance by scatter-hoarding rodents in deciduous forests – Ecology, 88: 2529-2540.
• [21] Murray A. L., Barber A. M., Jenkins S. H., Longland W. S. 2006 – Competitive environment affects food-hoarding behavior of merriam's kangaroo rats (Dipodomys merriami) – J. Mammal.87: 571-578.
• [22] Park S. J., Rhim S. J., Lee E. J., Lee W. S., Maguire C. C. 2014 – Home range, activity patterns, arboreality, and day refuges of the Korean Wood Mouse Apodemus peninsulae (Thomas, 1907) in a temperate forest in Korea – Mamm. Study.39, 209-217.
• [23] Preston S. D., Jacobs L. F. 2005 – Cache decision making: the effects of competition on cache decisions in Merriam's kangaroo rat (Dipodomys merriami) – J. Comp. Psychol.119: 187-196.
• [24] Rong K, Yang H, Ma J, Zong C, Cai T. 2013 – Food availability and animal space use both determine cache density of Eurasian red squirrels – PLoS ONE, 8: e80632.
• [25] Stapanian M. A., Smith C. C. 1978 – A model for seed scatter hoarding: coevolution of fox squirrels and black walnuts – Ecology, 59: 884-896.
• [26] Stapanian M. A., Smith C. C. 1984 – Density-dependent survival of scatter hoarded nuts: An experimental approach – Ecology, 65: 1387-1396.
• [27] Smith C. C., Follmer D. 1972 – Food preferences of squirrels – Ecology, 53: 82-91.
• [28] Smith C. C., Reichman O. J. 1984 – The evolution of food caching by birds and mammals – Annu. Rev. Ecol. Syst.15: 329-351.
• [29] Steele M. A., Bugdal M., Yuan A., Bartlow A., Buzalewski J., Lichti N.et al. 2011 – Cache placement, pilfering, and a recovery advantage in a seed-dispersing rodent: Could predation of scatter hoarders contribute to seedling establishment? – Acta Oecol.37: 554-560.
• [30] Steele M. A., Contreras T. A., Hadjchikh L. Z., Agosta S. J., Smallwood P. D., Tomlinson C. N. 2014 – Do scatter hoarders trade off increased predation risks for lower rates of cache pilferage? – Behav. Ecol.25: 206-215.
• [31] Thompson J. N. 2006 – Mutualistic webs of species – Science, 312: 372-373.
• [32] VanderWall S. B. 1990 – Food hoarding in animals – University of Chicago Press, Chicago, USA.
• [33] VanderWall S. B. 2001 – The evolutionary ecology of nut dispersal – Bot. Rev.67: 74-117.
• [34] Vander Wall S. B. 2010 – How plants manipulate the scatter-hoarding behaviour of seed-dispersing animals – Phil. Trans. R. Soc. B, 365: 989-997.
• [35] Vander Wall S. B., Beck M. J. 2012 – A comparison of frugivory and scatter-hoarding seed-dispersal syndromes – Bot. Rev.78: 10-31.
• [36] Vander Wall S. B., Jenkins S. H. 2003 – Reciprocal pilferage and the evolution of food-hoarding behavior – Behav. Ecol.14: 656-667.
• [37] Wang B., Chen J. 2009 – Seed size, more than nutrient or tannin content, affects seed caching behavior of a common genus of old world rodents – Ecology, 90: 3023-3032.
• [38] Wang B., Chen J. 2012 – Effects of fat and protein levels on foraging preferences of tannin in scatter-hoarding rodents – PLoS ONE, 7: e40640.
• [39] Wang B., Corlett R. T. 2017 – Scatter-hoarding rodents select different caching habitats for seeds with different traits – Ecosphere, 8: e01774.
• [40] Wang B., Ye C., Cannon C. H., Chen J. 2013 – Dissecting the decision making process of scatter-hoarding rodents – Oikos, 122: 1027-1034.
• [41] Willson M. F., Whelan C. J. 1990 – Variation in postdispersal survival of vertebrate-dispersed seeds: effects of density, habitat, location, season, and species – Oikos, 57: 191-198.
• [42] Xiao Z., Chang G., Zhang Z. 2008 – Testing the high-tannin hypothesis with scatter-hoarding rodents: experimental and field evidence – Anim. Behav.75: 1235-1241.
• [43] Xiao Z., Jansen P. A., Zhang Z. 2006b – Using seed-tagging methods for assessing post-dispersal seed fate in rodent-dispersed trees – Forest Ecol. Manag.223: 18-23.
• [44] Xiao Z., Wang Y., Harris M., Zhang Z. 2006a – Spatial and temporal variation of seed predation and removal of sympatric large-seeded species in relation to innate seed traits in a subtropical forest, southwest China – Forest Ecol. Manag.222: 46-54.
• [45] Xiao Z., Zhang Z. 2006 – Nut predation and dispersal of Harland Tanoak Lithocarpus harlandii, by scatter-hoarding rodents – Acta Oecol.29: 205-213.
• [46] Xiao Z., Zhang Z., Wang Y. 2005 – Effects of seed size on dispersal distance in five rodent-dispersed fagaceous species – Acta Oecol.28: 221-229.
• [47] Yang Y., Yi X., Niu K. 2012 – The effects of kernel mass and nutrition reward on seed dispersal of three tree species by small rodents – Acta Ethol.15: 1-8.
• [48] Yi X., Yang Y., Curtis R., Bartlow A. W., Agosta S. J., Steele M. A. 2012 – Alternative strategies of seed predator escape by early-germinating oaks in Asia and north America – Ecol. Evol.2: 487-492.
• [49] Yi X., Zhang Z. 2008 – Seed predation and dispersal of glabrous filbert (Corylusheterophylla) and pilose filbert (Corylus mandshurica) by small mammals in a temperate forest, northeast China – Plant Ecol.196: 135-142.
• [50] Zhang Y. F., Wang C., Tian S. L., Lu J. Q. 2014 – Dispersal and hoarding of sympatric forest seeds by rodents in a temperate forest from northern China – iForest: Biogeosciences and Forestry, 7: 70-74.

Uwagi

Opracowanie rekordu w ramach umowy 509/P-DUN/2018 ze środków MNiSW przeznaczonych na działalność upowszechniającą naukę (2019).