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Seed choice by rodents: learning or inheritance?

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Abstract

Learning plays a central role in animal life, and it has received special attention in the context of foraging. In this study, we have tested whether learning operates in seed choices by rodents using the Algerian mouse (Mus spretus) and Holm oak (Quercus ilex) acorns as a model. At the laboratory, those rodents captured in the field during the acorn fall period (experienced individuals) rejected weevil-infested acorns, presumably because of their lower energetic value. By contrast, rodents born in captivity and reared without any contact with acorns (naïves) predated weevil-infested acorns at similar rates than sound ones. After exposing naïves to infested and sound acorns during 15 days, they rejected infested acorns as the experienced individuals. In the field, predation on weevil-infested acorns was lower than on sound ones. Predation rates on infested acorns were lowest at the end of the acorn fall season, whereas predation rates of sound acorns increased along the same period. This might be explained by the improved ability to reject infested acorns because of the accumulated experience acquired by the initially naïve rodents along the acorn fall season. We show that learning shapes strongly seed choices by rodents, and it may be advantageous over inherited behaviors in variable unpredictable situations, such as acorn infestation rates that vary strongly between years and trees. We consider that the role of learning has to be taken into account in future studies on seed predation by rodents.

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References

  • Alcántara JM, Rey PJ, Sanchez-Lafuente AM, Valera F (2000) Early effects of rodent post-dispersal seed predation on the outcome of the plant-seed disperser interaction. Oikos 88:362–370

    Article  Google Scholar 

  • Alves C, Chichery R, Boal JG, Ludovic D (2007) Orientation in the cuttlefish Sepia officinalis: response versus place learning. Anim Cogn 10:29–36

    Article  PubMed  Google Scholar 

  • Beltman JB, Haccou P, ten Cate C (2004) Learning and colonization of new niches: a first step toward speciation. Evolution 58:35–46

    PubMed  Google Scholar 

  • Bernays EA, Bright KL (2005) Distinctive flavors improve foraging efficiency in the polyphagous grasshopper, Taeniopoda eques. Anim Behav 69:463–469

    Article  Google Scholar 

  • Blanco JC (1998) Mamíferos de España, vol. II. Editorial Planeta S. A., Barcelona

    Google Scholar 

  • Blate GM, Peart DR, Leighton M (1998) Post-dispersal predation on isolated seeds: a comparative study of 40 tree species in a Southeast Asian rainforest. Oikos 82:522–538

    Article  Google Scholar 

  • Bonal R, Muñoz A (2007) Multitrophic effects of ungulate intraguild predation on acorn weevils. Oecologia 152:533–540

    Article  PubMed  Google Scholar 

  • Bonal R, Muñoz A (2008) Seed growth suppression constrains the growth of seed parasites: premature acorn abscission reduces Curculio elephas larval size. Ecol Entomol (in press)

  • 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 

  • Brewer SW (2001) Predation and dispersal of large and small seeds of a tropical palm. Oikos 92:245–255

    Article  Google Scholar 

  • Brewer SW, Webb MAH (2001) Ignorant seed predators and factors affecting the postdispersal seed survival of the tropical palm Astrocaryum mexicanum. Oikos 93:32–41

    Article  Google Scholar 

  • Caldwell CA, Whiten A (2002) Evolutionary perspectives on imitation: is a comparative psychology of social learning possible? Anim Cogn 5:193–208

    Article  PubMed  Google Scholar 

  • Christensen KM, Whitman TG (1991) Indirect herbivore mediation of avian seed dispersal in Pinyon Pine. Ecology 72:534–542

    Article  Google Scholar 

  • Crawley MJ, Long CR (1995) Alternate bearing, predator satiation and seedling recruitment in Quercus robur L. J Ecol 83:683–696

    Article  Google Scholar 

  • Darmaillacq AS, Dickel L, Chichery MP, Agin V, Chichery R (2004) Rapid taste aversion learning in adult cuttlefish, Sepia officinalis. Anim Behav 68:1291–1298

    Article  Google Scholar 

  • Desouhant E, Debouzie D, Ploye H, Menu F (2000) Clutch size manipulations in the chestnut weevil, Curculio elephas: fitness of oviposition strategies. Oecologia 122:493–499

    Article  Google Scholar 

  • Dixon MD, Johnson WC, Adkisson CS (1997) Effects of weevil larvae on acorn use by blue jays. Oecologia 111:201–208

    Article  Google Scholar 

  • Dukas R (1998) Cognitive ecology. University of Chicago Press, Chicago

    Google Scholar 

  • Dukas R (2004) Evolutionary biology of animal cognition. Annu Rev Ecol Syst 35:347–374

    Article  Google Scholar 

  • Emery NJ, Dally JM, Clayton NS (2004) Western scrub-jays (Aphelocoma californica) use cognitive strategies to protect their caches from thieving conspecifics. Anim Cogn 7:37–43

    Article  PubMed  Google Scholar 

  • Emlen JM (1996) The role of time and energy in food preference. Am Nat 100:611–617

    Article  Google Scholar 

  • Estes JA, Riedman ML, Staedler MM, Tinker MT, Lyon BE (2003) Individual variation in prey selection by sea otters: patterns, causes and implications. J Anim Ecol 72:144–155

    Article  Google Scholar 

  • Forget PM (1990) Seed-dispersal of Vouacapoua americana (Caesalpiniaceae) by cavimorph rodents in French Guiana. J Trop Ecol 6:459–468

    Article  Google Scholar 

  • Gagliardo A, Ioale P, Odetti F, Bingman VP (2001) The ontogeny of the homing pigeon navigational map: evidence for a sensitive learning period. Proc R Soc Lond B 268:197–202

    Article  CAS  Google Scholar 

  • Galef BJ Jr (1996) Social enhancement of food preferences in Norway rats: a brief review. In: Heyes CM, Galef BJ Jr (eds) Social learning and imitation: the roots of culture. Academic, New York, pp 49–64

    Google Scholar 

  • Galef Jr BG , Whiskin EE (1998) Limits on social influence on food choices of Norway rats. Anim Behav 56:1015–1020

    Article  Google Scholar 

  • Galef BJ Jr, Giraldeau L-A (2001) Social influences on foraging in vertebrates: causal mechanisms and adaptative functions. Anim Behav 61:3–15

    Article  PubMed  Google Scholar 

  • Galef BG Jr, Whiskin EE (2001) Interaction of social and individual learning in food preferences of Norway rats. Anim Behav 62:41–46

    Article  Google Scholar 

  • Galef BG Jr, Whiskin EE (2004) Effects of environmental stability and demonstrator age on social learning of food preferences by young Norway rats. Anim Behav 68:897–902

    Article  Google Scholar 

  • Garb J, Kotler BP, Brown JS (2000) Foraging and comunity consequences of seed size for coexisting Negev Desert granivores. Oikos 88:291–300

    Article  Google Scholar 

  • García D, Gomez JM, Zamora R, Hodar JA (2000) Do empty Juniperus communis seeds defend filled seeds against predation by Apodemus sylvaticus? Ecoscience 7:214–221

    Google Scholar 

  • Guimaraes PR, Jose J, Galetti M, Trigo JR (2003) Quinolizidine alkaloids in Ormosia arborea seeds inhibit predation but not hoarding by agoutis (Dasyprocta leporina). J Chem Ecol 29:1065–1072

    Article  PubMed  CAS  Google Scholar 

  • Hadj-Chikh LZ, Steele MA, Smallwood PD (1996) Caching decisions by grey squirrels: a test of the handling time and perishability hypotheses. Anim Behav 52:941–948

    Article  Google Scholar 

  • Hayes JP, Jenkins SH (1997) Individual variation in mammals. J Mammal 78:274–293

    Article  Google Scholar 

  • Heisey DM (1985) Analyzing selection experiments with log-linear models. Ecology 66:1744–1748

    Article  Google Scholar 

  • Jacobs LF (1992) The effect of handling time on the decision to cache by gray squirrels. Anim Behav 43:522–524

    Article  Google Scholar 

  • Jansen PA, Bartholomeus M, Bongers F, Elzinga JA, den Ouden J, Van Wieren SE (2002) The role of seed size in dispersal by a scatter-hoarding rodent. In: Levey DJ, Silva WR, Galetti M (eds) Seed dispersal and frugivory: ecology, evolution and conservation. CAB International, Wallingford, pp 209–225

    Google Scholar 

  • Jenkins SH (1997) Perspectives on individual variation in mammals. J Mammal 78:271–273

    Google Scholar 

  • Kelley JL, Evans JP, Ramnarine IW, Magurran AE (2003) Back to school: can antipredator behaviour in guppies be enhanced through social learning? Anim Behav 65:655–662

    Article  Google Scholar 

  • Kollmann J, Coomes DA, White SM (1998) Consistencies in post-dispersal seed predation of temperate fleshy-fruited species among seasons, years and sites. Funct Ecol 12:683–690

    Article  Google Scholar 

  • Lachlan RF, Servedio MR (2004) Song learning accelerates allopatric speciation. Evolution 58:2049–2063

    PubMed  CAS  Google Scholar 

  • Leduc AOHC, Roh E, Breau C, Brown GE (2007) Learned recognition of a novel odour by wild juvenile Atlantic salmon, Salmo salar, under fully natural conditions. Anim Behav 73:471–477

    Article  Google Scholar 

  • Leiva MJ, Fernández-Ales R (2003) Post-dispersive losses of acorns from Mediterranean savannah-like forests and shrublands. For Ecol Manag 176:265–271

    Article  Google Scholar 

  • Muñoz A (2005) Ecological analyses of the predator and dispersal behaviour of Algerian mice (Mus spretus) and wood mice (Apodemus sylvaticus) foraging on Holm oak (Quercus ilex) acorns. Ph.D. thesis, Universidad Complutense de Madrid, Spain

  • Muñoz A, Bonal R (2007) Rodents change acorn dispersal behaviour in response to ungulate presence. Oikos 116:1631–1638

    Article  Google Scholar 

  • Pulido FJ, Díaz M (2005) Regeneration of a Mediterranean oak: a whole-cycle approach. Ecoscience 12:92–102

    Article  Google Scholar 

  • Qvarnstrom A, Blomgren V, Wiley C, Svedin N (2004) Female collared flycatchers learn to prefer males with an artificial novel ornament. Behav Ecol 15:543–548

    Article  Google Scholar 

  • Real LA (1993) Toward a cognitive ecology. Trends Ecol Evol 8:413–417

    Article  Google Scholar 

  • Roth JK, Vander Wall SB (2005) Primary and secondary seed dispersal of a bush chinquapin (Fagaceae) by scatterhoarding rodents. Ecology 86:2428–2439

    Article  Google Scholar 

  • Rowe C, Skelhorn J (2005) Colour biases are a question of taste. Anim Behav 69:587–594

    Article  Google Scholar 

  • Sallabanks R (1993) Hierarchical mechanisms of fruit selection by an avian frugivore. Ecology 74:1326–1336

    Article  Google Scholar 

  • Sallabanks R, Courtney SP (1992) Frugivory, seed predation and insect-vertebrate interactions. Annu Rev Entomol 37:377–400

    Article  PubMed  CAS  Google Scholar 

  • Semel B, Andersen DC (1988) Vulnerability of acorn weevils (Coleoptera: Curculionidae) and attractiveness of weevils and infested Quercus alba acorns to Peromyscus leucopus and Blarine brevicauda. Am Midl Nat 119:385–393

    Article  Google Scholar 

  • Shettleworth SJ (1998) Cognition, evolution, and behavior. Oxford University Press, New York

    Google Scholar 

  • Shettleworth SJ (2001) Animal cognition and animal behaviour. Anim Behav 61:277–286

    Article  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, Hadj-Chikh LZ, Hazeltine J (1996) Caching and feeding decisions by Sciurus carolinensis: responses to weevil-infested acorns. J Mammal 77:305–314

    Article  Google Scholar 

  • Steele MA, Manierre S, Genna T, Contreras TA, Smallwood PD, Pereira ME (2006) The innate basis of food-hoarding decisions in grey squirrels: evidence for behavioural adaptations to the oaks. Anim Behav 71:155–160

    Article  Google Scholar 

  • Stephens DW, Krebs JR (1986) Foraging theory. Princeton University Press, Princeton, NJ

    Google Scholar 

  • ten Cate C (2000) How learning mechanisms might affect evolutionary processes. Trends Ecol Evol 15:179–181

    Article  PubMed  Google Scholar 

  • Traveset A, Willson MF, Gaither Jr JC (1995) Avoidance by birds of insect-infested fruits of Vaccinium ovalifolium. Oikos 73:381–386

    Article  Google Scholar 

  • Vander Wall SB (1990) Food hoarding in animals. University of Chicago Press, Chicago

    Google Scholar 

  • Villalba JJ, Provenza FD, Han GD (2004) Experience influences diet mixing by herbivores: implications for plant biochemical diversity. Oikos 107:100–109

    Article  CAS  Google Scholar 

  • Weckerly FW, Nicholson KE, Semlitsch RD (1989) Experimental test of discrimination by Squirrels for insect-infested and non-infested acorns. Am Midl Nat 122:412–415

    Article  Google Scholar 

  • Wenny DG (2002) Effects of human handling of seeds on seed removal by rodents. Am Midl Nat 147:404–408

    Article  Google Scholar 

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Acknowledgments

We thank B. Nicolau for his assistance in the field and laboratory. M. Díaz, JM Aparicio, T Czeschlik, and three anonymous reviewers provided helpful comments on the manuscript. AM and RB were supported by a fellowship from La Junta de Comunidades de Castilla-La Mancha. This study was supported by the projects REN2003-07048/GLO, CGL2006-06647/BOS, PAC-02-008, 096/2002 and 003/2007. Rodents were captured and maintained in the laboratory under license from the JCCM.

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Correspondence to Alberto Muñoz.

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Communicated by T. Czeschlik

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

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