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Risk for the natural regeneration of Quercus species due to the expansion of rodent species (Microtus arvalis)

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Abstract

The role played by rodents in the colonization of acorn-producing plant species has been interpreted in different ways along time. It has gone from a predation relationship, in which rodents destroy seeds by devouring them, to a mutualistic one, in which they leave part of their caches or, more recently consume part of the cotyledons but leave the embryo intact. We studied how three rodent species, Apodemus sylvaticus (wood mouse), Mus spretus (Algerian mouse), and Microtus arvalis (common vole) treat the acorns they consume. The wood mouse and the Algerian mouse have consumed acorns for a long time and participate in this mutualistic relationship by preserving the embryo. The common vole eats acorns for the first time, as it is not a part of its habitual diet. We observed that this rodent species devours the embryo, as opposed to the other two rodent species that usually eat acorns and modifies its behavior over time, suggesting that its way of eating the acorns is not genetically fixed. The common vole has only recently started to enter the distribution areas of Quercus species. Its population density is high during certain periods, reaching plague levels in crops. When its usual food source runs out during these periods, it has to find others which probably include acorns. This rodent species eliminates the embryo during consumption and can, therefore, become a serious problem for acorn-producing species by limiting their colonization process. The three rodent species under study showed the same preference for the Quercus species provided, rejecting acorns of Q. suber and preferring those of Q. ilex subsp. ballota.

Significance statement

Microtus arvalis (common vole) is considered as an expansive crop pest species in certain parts of Europe, and in comparison with Apodemus sylvaticus (wood mouse) and Mus spretus (Algerian mouse), it does not have co-evolutionary history with Quercus species. Thus, the common vole is suggested to lack a mutualistic relationship with Quercus species where trees benefit from seed-dispersing rodents who then use parts of acorns as a food source. Using laboratory breeding, we showed that two habitual acorn consumers rodent species (wood mouse and Algerian mouse) tend to preserve the acorn embryo, while the expansive common vole that does not include acorns in its diet tend to eat the embryo. We concluded that the feeding behavior of the two habitual acorn consumer benefit the mutualistic relation with Quercus, probably due to the results of natural selection, whereas the expansive species not accustomed to eating acorns would impose a high risk to the natural regeneration of Quercus species.

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References

  • Beck MJ, Vander Wall SB (2010) Seed dispersal by scatter-hoarding rodents in arid environments. J Ecol 98:1300–1309

    Article  Google Scholar 

  • Bonal R, Muñoz A, Díaz M (2007) Satiation of predispersal seed predators: the importance of considering both plant and seed levels. Evol Ecol 21:367–380

    Article  Google Scholar 

  • Chang C, Xiao Z, Zhang Z (2009) Hoarding decisions by Edward’s long-tailed rats (Leopoldamys edwardsi) and South China field mice (Apodemus draco): the responses to seed size and germination schedule in acorns. Behav Process 82:7–11

    Article  Google Scholar 

  • De Blas C, Mateos GG, Rebollar PG (2003) Spanish Foundation for the development of animal nutrition. Madrid, Spain

  • Del Arco JM, Carretero M (2013) Preferencias en el consumo de bellotas por Mus spretus Lataste (1883) y su influencia en la dispersión de especies quercíneas (preferences in the consumption of acorns by Mus spretus Lataste (1883) and their influence on the dispersion of oaks species). In: Martínez C, Lario FJ, Fernández B (eds) Advances in the restoration of forest systems: implantation techniques. SECF-AEET. Palencia, Spain, pp 95–100

    Google Scholar 

  • Hou XG, Yi XF, Yang YQ, Liu WJ (2010) Acorn germination and seedling survival of Q. variabilis: effects of cotyledon excision. Ann For Sci 67:1–7. https://doi.org/10.1051/forest/2010036

    Article  Google Scholar 

  • Lichti NI, Steele MA, Swihart RK (2017) Seed fate and decision-making processes in scatter-hoarding rodents. Biol Rev 92:474–504. https://doi.org/10.1111/brv.12240

    Article  PubMed  Google Scholar 

  • Luque-Larena JJ, Mougeot F, Viñuela J, Jareño D, Arroyo L, Lambin X, Arroyo B (2013) Recent large-scale range expansion and outbreaks of the common vole (Microtus arvalis) in NW Spain. Basic Appl Ecol 14:432–441. https://doi.org/10.1016/j.baae.2013.04.006

    Article  Google Scholar 

  • Morán-López T, Fernández M, Alonso CL, Flores-Rentería D, Valladares F, Díaz M (2015) Effects of forest fragmentation on the oak–rodent mutualism. Oikos 124:1482–1491. https://doi.org/10.1111/oik.02061

    Article  Google Scholar 

  • Muñoz A, Bonal R (2008a) Are you strong enough to carry that seed? Seed size/body size ratios influence seed choices by rodents. Anim Behav 76:709–715

    Article  Google Scholar 

  • Muñoz A, Bonal R (2008b) Seed choice by rodents: learning or inheritance? Behav Ecol Sociobiol 62:913–922. https://doi.org/10.1007/s00265-007-0515-y

    Article  Google Scholar 

  • Muñoz A, Bonal R (2011) Linking seed dispersal to cache protection strategies. J Ecol 99:1016–1025

    Article  Google Scholar 

  • Muñoz A, Bonal R, Espelta J (2012) Responses of a scatter-hoarding rodent to seed morphology: links between seed choices and seed variability. Anim Behav 84:1435–1442

    Article  Google Scholar 

  • Paz A, Jareño D, Arroyo L, Viñuela J, Arroyo B, Mougeot F, Luque-Larena JJ, Fargallo JA (2012) Avian predators as a biological control system of common vole (Microtus arvalis) populations in North-Western Spain: experimental set-up and preliminary results. Pest Manag Sci 69:444–450. https://doi.org/10.1002/ps.3289

    Article  CAS  PubMed  Google Scholar 

  • Peguero G, Bonal R, Espelta JM (2014) Variation of predator satiation and seed abortion as seed defense mechanisms across an altitudinal range. Basic Appl Ecol 15:269–276

    Article  Google Scholar 

  • Perea R, San Miguel A, Gil L (2011a) Flying vs. climbing: factors controlling arboreal seed removal in oak-beech forests. For Ecol Manag 262:1251–1257

    Article  Google Scholar 

  • Perea R, San Miguel A, Gil L (2011b) Leftovers in seed dispersal: ecological implications of partial seed consumption for oak regeneration. J Ecol 99:94–201

    Article  Google Scholar 

  • Perea R, San Miguel A, Martínez-Jauregui M, Valbuena-Carabaña M, Gil L (2012) Effects of seed quality and seed location on the removal of acorns and beechnuts. Eur J For Res 131:632–631. https://doi.org/10.1007/s10342-011-0536-y

    Article  Google Scholar 

  • Perea R, Girardello M, San Miguel A (2014) Big game or big loss? High deer densities are threatening woody plant diversity and vegetation dynamics. Biodivers Conserv 23:1303–1318

    Article  Google Scholar 

  • Perea R, Dirzo R, San Miguel A, Gil L (2016) Post-dispersal seed recovery by animals: is it a plant or an animal-driven process? Oikos 125:1203–1210. https://doi.org/10.1111/oik,02556

    Article  Google Scholar 

  • Pérez-Ramos IM, Marañón T (2008) Factors affecting post-dispersal seed predation in two coexisting oak species: microhabitat, burial and exclusion of large herbivores. For Ecol Manag 255:3506–3514

    Article  Google Scholar 

  • Pérez-Ramos IM, Verdú JR, Numa C, Marañón T, Lobo JM (2013) The comparative effectiveness of rodents and dung beetles as local seed dispersers in Mediterranean oak forests. PLoS One 8:77197. https://doi.org/10.1371/journal.pone.0077197

    Article  CAS  Google Scholar 

  • Pinheiro J, Bates D (2000) Mixed-effects models in S and S-plus. Springer, New York

    Book  Google Scholar 

  • Pinheiro J, Bates D, DebRoy S, Sarkar D, The R Development Core Team (2013) nlme: linear and nonlinear mixed effects models. R Package Version 3:1–108 https://CRAN.R-project.org/package=nlme

    Google Scholar 

  • Pons J, Pausas JG (2007) Rodent acorn selection in a Mediterranean oak landscape. Ecol Res 22:535–541

    Article  Google Scholar 

  • R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, http://www.R-project.org/

  • Sokal RR, Rohlf FJ (1995) Biometry, 3rd edn. W.H. Freeman and Co., New York

    Google Scholar 

  • Steele MA, Knowles T, Bridle K, Simms EL (1993) Tannins and partial consumption of acorns: implications for dispersal of oaks by seed predators. Am Midl Nat 130:229–238

    Article  Google Scholar 

  • Steele MA, Turner G, Smallwood PD, Wolff JO, Radillo J (2001) Cache management by small mammals: experimental evidence for the significance of acorn-embryo excision. J Mammal 82:35–38

    Article  Google Scholar 

  • Sundaram M, Willoughby JR, Lichti NI, Steele MA, Swihart RK (2015) Segregating the effects of seed traits and common ancestry of hardwood trees on eastern gray squirrel foraging decisions. PLoS One 10:e0130942. https://doi.org/10.1371/journal.pone.0130942

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sunyer P, Espelta JM, Bonal R, Munoz A (2014) Seeding phenology influences wood mouse seed choices: the overlooked role of timing in the foraging decisions by seed-dispersing rodents. Behav Ecol Sociobiol 68:1205–1213

    Article  Google Scholar 

  • Vander Wall SB (2001) The evolutionary ecology of nut dispersal. Bot Rev 67:74–117

    Article  Google Scholar 

  • Vander Wall SB (2010) How plants manipulate the scatter-hoarding behaviour of seed-dispersing animals. Philos Trans R Soc B 365:989–997

    Article  Google Scholar 

  • Xiao Z, Krebs CJ (2015) Modeling the costs and benefits of seed scatter-hoarding to plants. Ecosphere 6:1–8. https://doi.org/10.1890/ES14-00438.1

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Xiao Z, Gao X, Jiang M, Zhang Z (2009) Behavioural adaptation of Pallas’s squirrels to germination schedule and tannins in acorns. Behav Ecol 20:1050–1055. https://doi.org/10.1093/beheco/arp096

    Article  Google Scholar 

  • Yang Y, Yi X (2012) Partial acorn consumption by small rodents: implication for regeneration of white oak Quercus mongolica. Plan Ecol 213:197–205

    Article  Google Scholar 

  • Yi X, Yang Y, Curtis R, Bartlow AW, Agosta S, Steele MA (2012) Alternative strategies of seed predator escape by early-germinating oaks in Asia and North America. Ecol Evol 2:487–492

    Article  Google Scholar 

  • Yi X, Curtis R, Bartlow AW, Agosta SJ, Steele MA (2013) Ability of chestnut oak to tolerate acorn pruning by rodents. The role of the cotyledonary petiole. Naturwissenschaften 100:81–90. https://doi.org/10.1007/s00114-012-0996-z

    Article  CAS  PubMed  Google Scholar 

  • Yi X, Wang Z, Liu C, Liu G, Zhang M (2015) Acorn cotyledons are larger than their seedlings’ need: evidence from artificial cutting experiments. Sci Rep 5:8112. https://doi.org/10.1038/srep08112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang H, Zhang Z (2008) Endocarp thickness affects seed removal speed by small rodents in a warm-temperate broad-leafed deciduous forest China. Act Oecol 34:285–293

    Article  Google Scholar 

  • Zhang M, Steele MA, Yi X (2013) Reconsidering the effects of tannin on seed dispersal by rodents: evidence from enclosure and field experiments with artificial seeds. Behav Process 100:200–207

    Article  Google Scholar 

  • Zhang M, Dong Z, Yi X, Bartlow AW (2014) Acorns containing deeper plumule survive better: how white oaks counter embryo excision by rodents. Ecol Evol 4:59–66

    Article  Google Scholar 

Download references

Acknowledgments

We thank Junta de Castilla y León for permission granted to carry out this research, in their mission to safeguard ethics in animal welfare during their handling. We thank Ángel José Álvarez Barcia, the director of S.I.B.A. (Servicio de Investigación y Bienestar Animal) at the University of Valladolid, for his advice on correct treating and handling of rodents. We also thank the associate editor, Prof. Erkki Korpimäki, two anonymous reviewers, and Dr. Pilar Zaldívar and Dr. Ángel Hernández for their valuable comments to improve the manuscript.

Funding

This study was partially supported by the Projects VA002A07 and VA035G18 from Junta de Castilla y León to JMDA.

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Correspondence to Jose María Del Arco.

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The authors declare that they have no conflict of interest.

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All applicable international guidelines for the care and use of animals were followed. All procedures performed in this study involving animals were in accordance with the ethical standards of the institution at which the studies were conducted (CEEBA University of Valladolid, Spain). The experimental procedures were designed in accordance with the requirements of replacement, reduction and refinement.

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Communicated by E. Korpimäki

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Del Arco, J.M., Beltrán, D. & Martínez-Ruiz, C. Risk for the natural regeneration of Quercus species due to the expansion of rodent species (Microtus arvalis). Behav Ecol Sociobiol 72, 160 (2018). https://doi.org/10.1007/s00265-018-2575-6

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  • DOI: https://doi.org/10.1007/s00265-018-2575-6

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