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Plant Secondary Metabolites as Rodent Repellents: a Systematic Review

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Abstract

The vast number of plant secondary metabolites (PSMs) produced by higher plants has generated many efforts to exploit their potential for pest control. We performed a systematic literature search to retrieve relevant publications, and we evaluated these according to PSM groups to derive information about the potential for developing plant-derived rodent repellents. We screened a total of 54 publications where different compounds or plants were tested regarding rodent behavior/metabolism. In the search for widely applicable products, we recommend multi-species systematic screening of PSMs, especially from the essential oil and terpenoid group, as laboratory experiments have uniformly shown the strongest effects across species. Other groups of compounds might be more suitable for the management of species-specific or sex-specific issues, as the effects of some compounds on particular rodent target species or sex might not be present in non-target species or in both sexes. Although plant metabolites have potential as a tool for ecologically-based rodent management, this review demonstrates inconsistent success across laboratory, enclosure, and field studies, which ultimately has lead to a small number of currently registered PSM-based rodent repellents.

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References

  • Adeyemi MMH (2010) The potential of secondary metabolites in plant material as deterrents against insect pests: a review. African J. Pure Appl Chem 4:243–246

    CAS  Google Scholar 

  • Apfelbach R, Blanchard CD, Blanchard RJ, Hayes RA, McGregor IS (2005) The effects of predator odors in mammalian prey species: a review of field and laboratory studies. Neurosci Biobehav Rev 29:1123–1144

    Article  PubMed  Google Scholar 

  • Babbar BK, Kaur J, Singla N, Mahal AK (2015) Effectiveness and persistence of cinnamic aldehyde as an antifeedant on rats under storage conditions. Crop Prot 67:235–242

    Article  CAS  Google Scholar 

  • Baker SE, Johnson PJ, Slater D, Watkins RW, Macdonald DW (2007) Learned food aversion with and without an odour cue for protecting untreated baits from wild mammal foraging. Appl Anim Behav Sci 102:410–428

    Article  Google Scholar 

  • Barthelmess EL (2001) The effects of tannin and protein on food preference in eastern grey squirrels. Ethol Ecol Evol 13:115–132

    Article  Google Scholar 

  • Basey JM, Jenkins SH, Busher PE (1988) Optimal central-place foraging by beavers: tree-size selection in relation to defensive chemicals of quaking aspen. Oecologia 76:278–282

    Article  Google Scholar 

  • Basey JM, Jenkins SH, Miller GC (1990) Food selection by beavers in relation to inducible defenses of Populus tremuloides. Oikos 59:57–62

    Article  Google Scholar 

  • Bell CMC, Rarestad A, Harestad AS (1987) Efficacy of pine oil as repellent to wildlife. J Chem Ecol 13:1409–1417

    Article  CAS  PubMed  Google Scholar 

  • Bennett RN, Wallsgrove RM (1994) Secondary metabolites in plant defence mechanisms. New Phytol 127:617–633

    Article  CAS  Google Scholar 

  • Berenbaum MR (1991) Coumarins. In: Rosenthal GA, Berenbaum, MR (eds) Herbivores: Their Interaction with Secondary Plant Metabolites. Volume I: Chemical Participants. Academic Press, London, pp 221–244

  • Bergeron JM, Jodoin L (1991) Costs of nutritional constraints on the vole (Microtus pennsylvanicus) along a time gradient. Can J Zool 69:1496–1503

    Article  Google Scholar 

  • Bordes F, Blasdell K, Morand S (2015) Transmission ecology of rodent-borne diseases: New frontiers. Integr Zool 10:424–435

    Article  PubMed  Google Scholar 

  • Boyle R, Dearing MD (2003) Ingestion of juniper foliage reduces metabolic rates in woodrat (Neotoma) herbivores. Zoology 106:151–158

    Article  CAS  PubMed  Google Scholar 

  • Bozinovic F (1997) Diet selection in rodents: an experiment test of the effect of dietary fiber and tannins on feeding behavior. Rev Chil Hist Nat 70:67–71

    Google Scholar 

  • Bozinovic F, Novoa F, Sabat P (1997) Feeding and digesting fiber and tannins by an herbivorous rodent, Octodon degus (Rodentia: Caviomorpha). Comp Biochem Physiol - A Physiol 118:625–630

    Article  CAS  PubMed  Google Scholar 

  • Brooke McEachern M, Eagles-Smith CA, Efferson CM, Van Vuren DH (2006) Evidence for local specialization in a generalist mammalian herbivore, Neotoma fuscipes. Oikos 113:440–448

    Article  Google Scholar 

  • Brown PR, Singleton GR, Clark L, Watkins R (2000) Impacts of rodent pests on crops in Australia - costs and damage. Human Conflicts with Wildlife: Economics Considerations. National Wildlife Research Center, Colorado

  • Bryja J, Nesvadbová J, Heroldová M, Jánová E, Losík J, Trebatická L, Tkadlec E (2005) Common vole (Microtus arvalis) population sex ratio: biases and process variation. Can J Zool 83:1391–1399

    Article  Google Scholar 

  • Buckle AP, Smith RH (2015) Rodent pests and their control, 2nd edn. CABI, London

    Google Scholar 

  • Cheynier V, Comte G, Davies KM, Lattanzio V, Martens S (2013) Plant phenolics: recent advances on their biosynthesis, genetics, and ecophysiology. Plant Physiol Biochem 72:1–20

    Article  CAS  PubMed  Google Scholar 

  • Crocker DR, Scanlon CB, Perry SM (1993) Repellency and choice: feeding responses of wild rats (Rattus norvegicus) to cinnamic acid derivatives. Appl Anim Behav Sci 38:61–66

    Article  Google Scholar 

  • Curtis PD, Rowland ED, Good GL (2002) Developing a plant-based vole repellent: screening of ten candidate species. Crop Prot 21:299–306

    Article  Google Scholar 

  • Dai X, Han M, Liu Q, Shan G, Yin B, Wang A, Dean BE, Wei W, Yang S (2014) Seasonal changes in the concentrations of plant secondary metabolites and their effects on food selection by Microtus oeconomus. Mamm Biol - Zeitschrift für Säugetierkd 79:215–220

    Article  Google Scholar 

  • Dearing D, Mangione AM, Karasov WH (2001) Plant secondary compounds as diuretics: an overlooked consequence. Am Zool 901:890–901

    Google Scholar 

  • Dearing MD, Foley WJ, McLean S (2005) The influence of plant secondary metabolites on the nutritional ecology of herbivorous terrestrial vertebrates. Annu Rev Ecol Evol Syst 36:169–189

    Article  Google Scholar 

  • DeGabriel JL, Moore BD, Felton AM, Ganzhorn JU, Stolter C, Wallis IR, Johnson CN, Foley WJ (2014) Translating nutritional ecology from the laboratory to the field: milestones in linking plant chemistry to population regulation in mammalian browsers. Oikos 123:298–308

    Article  Google Scholar 

  • Delattre P, Giraudoux P, Baudry J, Musard P, Toussaint M, Truchetet D, Stahl P, Poule ML, Artois M, Damange JP, Quéré JP (1992) Land use patterns and types of common vole (Microtus arvalis) population kinetics. Agric Ecosyst Environ 39:153–168

    Article  Google Scholar 

  • DelBarco-Trillo J, McPhee ME, Johnston RE (2011) Syrian hamster males below an age threshold do not elicit aggression from unfamiliar adult males. Aggress Behav 37:91–97

    Article  PubMed  Google Scholar 

  • DeTour for Rodents (2016). In: Front. Perform. Lubr. http://www.frontierlubricants.com/frontier-Lubricants-store/detour-for-rodents-single-10-oz-tube. Accessed 12 Jan 2016

  • Diawara MM, Kulkosky PJ (2003) Reproductive toxicity of the psoralens. Pediatr Pathol Mol Med 22:247–258

    Article  CAS  PubMed  Google Scholar 

  • Doungboupha B, Aplin KP, Singleton GR (2003) Rodent outbreaks in the uplands of Laos: analysis of historical patterns and the identity of nuu khii. ACIAR Monogr. Ser 96:103–111

    Google Scholar 

  • Eason CT, Murphy EC, Wright GRG, Spurr EB (2002) Assessment of risks of brodifacoum to non-target birds and mammals in New Zealand. Ecotoxicology 11:35–48

    Article  PubMed  Google Scholar 

  • Edlich S, Stolter C (2012) Effects of essential oils on the feeding choice by moose. Alces 48:17–25

    Google Scholar 

  • Epple G, Niblick H, Lewis S, Nolte DL, Campbell DL, Mason JR (1996) Pine needle oil causes avoidance behaviors in pocket gopher Geomys bursarius. J Chem Ecol 22:1013–1025

    Article  CAS  PubMed  Google Scholar 

  • Epple G, Bryant BP, Mezine I, Lewis S (2001) Zanthoxylum piperitum, an Asian spice, inhibits food intake in rats. J Chem Ecol 27:1627–1640

    Article  CAS  PubMed  Google Scholar 

  • Etscorn FT, Torres L (1997) Animal repellent. 3–5. https://www.google.com/patents/US5674496

  • Fanson BG, Fanson KV, Brown JS (2008) Foraging behaviour of two rodent species inhabiting a kopje (rocky outcrop) in Tsavo West National Park, Kenya. African Zool 43:184–191

    Article  Google Scholar 

  • Fedriani JM, Boulay R (2006) Foraging by fearful frugivores: combined effect of fruit ripening and predation risk. Funct Ecol 20:1070–1079

    Article  Google Scholar 

  • Fischer D, Pelz H-J, Prokop A (2009) The effect of secondary plant compounds for repelling water voles, Arvicola amphibius (previously Arvicola terrestris). Jul Kühn-Archiv 419:67–69

  • Fischer D, Jacob J, Prokop A, Wink M, Mattes H (2010) Sustainable measures against water voles: the repelling effect of secondary plant compounds against Arvicola amphibius. Jul Kühn-Archiv 77–78

  • Fischer D, Prokop A, Mattes M, Wink H, Jacob J (2011a) The repelling effect of secondary plant compounds against voles. Jul Kühn-Archiv 432:58–59

  • Fischer D, Prokop A, Wink M, Mattes M, Jacob J (2011b) Smell you later - the repelling effect of secondary plant compounds against water voles and. Jul Kühn-Archiv 432:159

  • Fischer D, Imholt C, Pelz HJ (2013a) The repelling effect of plant secondary metabolites on water voles, Arvicola amphibius. Pest Manag Sci 69:437–443

    Article  CAS  PubMed  Google Scholar 

  • Fischer D, Imholt C, Prokop A, Jacob J (2013b) Efficacy of methyl nonyl ketone as an in-soil repellent for common voles (Microtus arvalis. Pest Manag Sci 69:431–436

    Article  CAS  PubMed  Google Scholar 

  • Foley WJ (1992) Nitrogen and energy retention and acid-base status in the common ringtail possum (Pseudocheirus peregrinus): evidence of the effects of absorbed allelochemicals. Physiol Zool 65:403–421

    Article  CAS  Google Scholar 

  • Freeland WJ, Saladin LR (1989) Choice of mixed diets by herbivores: the idiosyncratic effects of plant secondary compounds. Biochem Syst Ecol 17:493–497

    Article  CAS  Google Scholar 

  • Garcia J, Kimeldorf DJ, Koelling RA (1955) Conditioned aversion to saccharin resulting from exposure to gamma radiation. Science 122:157–158

    CAS  PubMed  Google Scholar 

  • Geduhn A, Esther A, Schenke D, Mattes M, Jacob J (2014) Spatial and temporal exposure patterns in non-target small mammals during brodifacoum rat control. Sci Total Environ 496:328–338

    Article  CAS  PubMed  Google Scholar 

  • Geduhn A, Jacob J, Schenke D, Keller B, Kleinschmidt S, Esther A (2015) Relation between intensity of biocide practice and residues of anticoagulant rodenticides in red foxes (Vulpes vulpes). PLoS One 10:e0139191

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ghidiu G, Kuhar T, Palumbo J, Schuster D (2012) Drip chemigation of insecticides as a pest management tool in vegetable production. J Integr Pest Manag 3:1–5

    Article  Google Scholar 

  • Gill EL, Watkins RW, Gurney JE, Bishop JD (1995) Cinnamamide: a nonlethal chemical repellent for birds and mammals. National Wildlife Research Center Conference, Nebraska, pp. 43–51

    Google Scholar 

  • Grant-Hoffman MN, Barboza PS (2010) Herbivory in invasive rats: Criteria for food selection. Biol Invasions 12:805–825

    Article  Google Scholar 

  • Guimarães PR, José 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  Google Scholar 

  • Gurney JE, Watkins RW, Gill EL, Cowan DP (1996) Non-lethal mouse repellents: evaluation of cinnamamide as a repellent against commensal and field rodents. Appl Anim Behav Sci 49:353–363

    Article  Google Scholar 

  • Halaweish F, Kronberg S, Rice JA (2003) Rodent and ruminant ingestive response to flavonoids in Euphorbia esula. J Chem Ecol 29:1073–1082

    Article  CAS  PubMed  Google Scholar 

  • Hansen SC, Stolter C, Jacob J (2015) The smell to repel: the effect of odors on the feeding behavior of female rodents. Crop Prot 78:270–276

    Article  Google Scholar 

  • Hansen SC, Stolter C, Jacob J (2016) Effect of plant secondary metabolites on feeding behavior of microtine and arvicoline rodent species. J Pest Sci 84(4):955–963

  • Hartley SE, Nelson K, Gorman M (1995) The effect of fertilizer and shading on plant-chemical composition and palatability to Orkney voles, Microtus arvalis orcadensis. Oikos 72:79–87

    Article  Google Scholar 

  • Hjältén J, Palo T (1992) Selection of deciduous trees by free ranging voles and hares in relation to plant chemistry. Oikos 63:477–484

    Article  Google Scholar 

  • Howard W, Marsh R (1970) Olfaction in rodent control. Proceedings of the 4th Vertebrate Pest Conference. University of Nebraska, Davis, pp 64–70

  • Huang E (2014) Approved and banned rodenticides in China. In: ChemLinked. https://agrochemical.chemlinked.com/agro-analysisexpert-article/approved-and-banned-rodenticides-china. Accessed 12 Jan 2016

  • Iason GR, Villalba JJ (2006) Behavioral strategies of mammal herbivores against plant secondary metabolites: the avoidance-tolerance continuum. J Chem Ecol 32:1115–1132

    Article  CAS  PubMed  Google Scholar 

  • Iason GR, O’Reilly-Wapstra JM, Brewer MJ, Summers RW, Moore BD (2011) Do multiple herbivores maintain chemical diversity of Scots pine monoterpenes? Philos Trans R Soc Lond B Biol Sci 366:1337–1345

    Article  PubMed  PubMed Central  Google Scholar 

  • Jacob J, Buckle A (2016) Use of anticoagulant rodenticides in different applications around the world. In: van den Brink N, Elliott J, Shore R, Rattner B (eds) Impact of anticoagulant rodenticides on non-target wildlife (in press)

  • Jacob J, Rahmini, Sudarmaji (2006) The impact of imposed female sterility on field populations of ricefield rats (Rattus argentiventer). Agric Ecosyst Environ 115:281–284

    Article  Google Scholar 

  • Jacob J, Manson P, Barfknecht R, Fredricks T (2014) Common vole (Microtus arvalis) ecology and management: implications for risk assessment of plant protection products. Pest Manag Sci 70:869–878

    Article  CAS  PubMed  Google Scholar 

  • Janzen DH, Fellows LE, Waterman PG (1990) What protects Lonchocarpus (Leguminosae) seeds in a costa Rican dry forest? Biotropica 22:272–285

    Article  Google Scholar 

  • John A (2014) Rodent outbreaks and rice pre-harvest losses in Southeast Asia. Food Secur 6:249–260

    Article  Google Scholar 

  • Jung HJG, Batzli GO (1981) Nutritional ecology of microtine rodents:effects of plant extracts on the growth of arctic microtines. J Mammal 62:286–292

    Article  Google Scholar 

  • Kelsey RG, Forsman ED, Swingle JK (2009) Terpenoid resin distribution in conifer needles with implications for red tree vole, Arborimus longicaudus, foraging. Can Field-Naturalist 123:12–18

    Google Scholar 

  • Kettunen M, Genovesi P, Gollasch S, Pagad S, Starfinger U, Brink, ten P, Shine C (2009) Technical support to EU strategy on invasive alien species (IAS). Brussels

  • Kyriazakis I, Anderson DH, Duncan AJ (1998) Conditioned flavour aversions in sheep: the relationship between the dose rate of a secondary plant compound and the acquisition and persistence of aversions. Br J Nutr 79:55–62

    Article  CAS  PubMed  Google Scholar 

  • Laitinen J, Rousi M, Tahvanainen J, Henttonen H, Heinonen J (2004) The effects of nutrient variation and age on the resistance of three winter-dormant white birch species to mammalian herbivores. Can J For Res 34:2230–2239

    Article  Google Scholar 

  • Leirs H, Stenseth NC, Nichols JD, Hines JE, Verhagen R, Verheyen W (1997) Stochastic seasonality and nonlinear density-dependent factors regulate population size in an African rodent. Nature 389:176–180

    Article  CAS  PubMed  Google Scholar 

  • Levey DJ, Tewksbury JJ, Cipollini ML, Carlo TA (2006) A field test of the directed deterrence hypothesis in two species of wild chili. Oecologia 150:61–68

    Article  PubMed  Google Scholar 

  • Levin DA (1976) The chemical defenses of plants to pathogens and herbivores. Annu Rev Ecol Syst 7:121–159

    Article  CAS  Google Scholar 

  • Lindroth RL, Batzli GO (1986) Inducible plant chemical defences: a cause of vole population cycles? J Anim Ecol 55:431–449

    Article  Google Scholar 

  • Marsh KJ, Foley WJ, Cowling A, Wallis IR (2003) Differential susceptibility to Eucalyptus secondary compounds explains feeding by the common ringtail (Pseudocheirus peregrinus) and common brushtail possum (Trichosurus vulpecula). J Comp Physiol B 173:69–78

    CAS  PubMed  Google Scholar 

  • Marsh KJ, Wallis IR, Andrew RL, Foley WJ (2006) The detoxification limitation hypothesis: where did it come from and where is it going? J Chem Ecol 32(6):1247–1266

    Article  CAS  PubMed  Google Scholar 

  • Marsh KJ, Wallis IR, Foley WJ (2007) Behavioural contributions to the regulated intake of plant secondary metabolites in koalas. Oecologia 154:283–290

    Article  PubMed  Google Scholar 

  • Mason JR, Nolte DL, Bryant BP (1996) Effectiveness of thirteen vertebrate repellents as rodent trigeminal stimulants. Physiol Behav 6:1449–1452

    Article  Google Scholar 

  • McLean S, Duncan AJ (2006) Pharmacological perspectives on the detoxification of plant secondary metabolites: implications for ingestive behavior of herbivores. J Chem Ecol 32(6):1213–1228

    Article  CAS  PubMed  Google Scholar 

  • McLean S, Boyle RR, Brandon S, Davies NW, Sorensen JS (2007) Pharmacokinetics of 1,8-cineole, a dietary toxin, in the brushtail possum (Trichosurus vulpecula): significance for feeding. Xenobiotica 37:903–922

    Article  CAS  PubMed  Google Scholar 

  • Meerburg BG, Singleton GR, Kijlstra A (2009) Rodent-borne diseases and their risks for public health. Crit Rev Microbiol 35:221–270

    Article  PubMed  Google Scholar 

  • Meyer MW, Karasov WH (1989) Antiherbivore chemistry of Larrea Tridentata: effects on woodrat (Neotoma lepida) feeding and nutrition. Ecology 70:953–961

    Article  Google Scholar 

  • Moore BD, Foley WJ (2005) Tree use by koalas in a chemically complex landscape. Nature 435:488–490

    Article  CAS  PubMed  Google Scholar 

  • Nature’s defense (2010). In: Weiser Gr. Lcc. http://www.gemplers.com/docs/msds/B8275.pdf. Accessed 12 Jan 2016

  • Nerio LS, Olivero-Verbel J, Stashenko E (2010) Repellent activity of essential oils: a review. Bioresour Technol 101:372–378

    Article  CAS  PubMed  Google Scholar 

  • Nolte DL, Farley JP, Campbell DL, Epple G, Mason JR (1993) Potential repellents to prevent mountain beaver damage. Crop Prot 12:624–626

    Article  CAS  Google Scholar 

  • Nolte DL, Campbell DL, Mason JR (1994a) Potential repellents to reduce damage by herbivores. In: Halverson WS, Crabb AC (eds) Proceedings of the Sixteenth Vertebrate Pest Conference. University of California:Davis pp 228–232

  • Nolte DL, Mason JR, Epple G, et al. (1994b) Why are predator urines aversive to prey? J Chem Ecol 20:1505–1516

    Article  CAS  PubMed  Google Scholar 

  • Oerke E-C (2006) Crop losses to pests. J Agric Sci 144:31

    Article  Google Scholar 

  • Ostfeld RS, Canham CD (1995) Density-dependent processes in meadow voles: an experimental approach. Ecology 76:521–532

    Article  Google Scholar 

  • Palo RT, Robbins CT (1991) Plant defenses against mammalian herbivory. CRC Press, Boca Raton

    Google Scholar 

  • Provenza FD, Burritt EA, Clausen TP, Bryant JP, Reichardt PB (1990) Conditioned flavor aversion: a mechanism for goats to avoid condensed tannins in blackbrush. Am Nat 136:810–828

    Article  Google Scholar 

  • Provenza FD, Ortega-Reyes L, Scott CB, Lynch JJ, Burritt EA (1994) Antiemetic drugs attenuate food aversions in sheep. J Anim Sci 72:1989–1994

    CAS  PubMed  Google Scholar 

  • Rezsutek MJ, Cameron GN (2011) Diet selection and plant nutritional quality in Attwater’s pocket gopher (Geomys attwateri). Mamm Biol 76:428–435

    Google Scholar 

  • Rice P, Church D (1974) Taste responses of deer to browse extracts, organic acids, and odors. J Wildl Manag 38:830–836

    Article  CAS  Google Scholar 

  • Rosalino LM, Nóbrega F, Santos-Reis M, Teixeira G, Rebelo R (2013) Acorn selection by the wood mouse Apodemus sylvaticus: a semi-controlled experiment in a mediterranean environment. Zool Sci 30:724–730

    Article  PubMed  Google Scholar 

  • Rosenthal GA, Berenbaum MR (1991) Herbivores: their interactions with secondary plant metabolites: volume I: the chemical participants. Academic Press, London

    Google Scholar 

  • Roser M (2016) Land Use in Agriculture. Published online at OurWorldInData.org. https://ourworldindata.org/land-use-in-agriculture/ [Online Resource] Accessed 10 Aug 2016

  • Rousi M, Tahvanainen J, Henttonen H, Uotila I (1993) Effects of shading and fertilization on resistance of winter- dormant birch (Betula pendula) to voles and hares. Ecology 74:30–38

    Article  Google Scholar 

  • Rubino FM, Martinoli A, Pitton M, Di Fabio D, Caruso E, Banfi S, Tosi G, Wauters LA, Martinoli A (2012) Food choice of Eurasian red squirrels and concentrations of anti-predatory secondary compounds. Mamm Biol 77:332–338

    Google Scholar 

  • Samuni-Blank M, Izhaki I, Dearing MD, Gerchman Y, Trabelcy B, Lotan A, Karasov WH, Arad Z (2012) Intraspecific directed deterrence by the mustard oil bomb in a desert plant. Curr Biol 22:1218–1220

    Article  CAS  PubMed  Google Scholar 

  • Samuni-Blank M, Arad Z, Dearing MD, Gerchman Y, Karasov WH, Izhaki I (2013a) Friend or foe? Disparate plant-animal interactions of two congeneric rodents. Evol Ecol 27:1069–1080

    Article  Google Scholar 

  • Samuni-Blank M, Izhaki I, Dearing MD, Karasov WH, Gerchman Y, Kohl KD, Lymberakis P, Kurnath P, Arad Z (2013b) Physiological and behavioural effects of fruit toxins on seed-predating versus seed-dispersing congeneric rodents. J Exp Biol 216:3667–3673

    Article  CAS  PubMed  Google Scholar 

  • Samuni-Blank M, Izhaki I, Gerchman Y, Dearing MD, Karasov WH, Trabelcy B, Edwards TM, Arad Z (2014) Taste and physiological responses to glucosinolates: seed predator versus seed disperser. PLoS One 9:4–9

    Google Scholar 

  • Saunders GR (1983) Evaluation of mouse-plague control techniques in irrigated sunflower crops. Crop Prot 2:437–445

    Article  CAS  Google Scholar 

  • Schmidt KA, Brown JS, Morgan RA (1998) Plant defenses as complementary resources: a test with squirrels. Oikos 81:130–142

    Article  Google Scholar 

  • Seigler DS (1991) Cyanide and cyanogenic glycosides. In: Rosenthal GA, Berenbaum MR (eds) Herbivores: Their Interactions with Secondary Plant Metabolites. Volume I: Chemical Participants. Academic Press, pp 35–77

  • Shaw RF, Pakeman RJ, Young MR, Iason GR (2013) Microsite affects willow sapling recovery from bank vole (Myodes glareolus) herbivory, but does not affect grazing risk. Ann Bot 112:731–739

    Article  PubMed  PubMed Central  Google Scholar 

  • Shumake SA, Hakim A (2000) Evaluating Norway rat response to attractant and repellant odors to improve rodenticide baiting effectiveness. In: Brittingham, MC, Kays J, McPeake R (eds) The 9th Wildlife Damage Management Conference Proceedings. State College, pp 103–110

  • Singleton GR, Brown PR (2005) One hundred years of eruptions of house mice in Australia–a natural biological curio. Biol J Linn Soc 84:617–627

    Article  Google Scholar 

  • Singleton GR, Leirs H, Hinds LA, Zhang ZB (1999) Ecologically-based management of rodent pests-re-evaluating our approach to an old problem. Canberra

  • Singleton GR, Sudarmaji Tuan NP, Sang PM, Huan NH, Brown PR, Jacob J, Heong KL, Escalada MM (2003) Reduction in chemical use following integrated ecologically based rodent management. Int Rice Res Notes 28:33–35

    Google Scholar 

  • Singleton GR, Brown PR, Jacob J, Aplin KP (2007) Unwanted and unintended effects of culling: a case for ecologically-based rodent management. Integr Zool 2:247–259

    Article  PubMed  Google Scholar 

  • Singleton GR, Belmain SR, Brown PR, Hardy B (2010) Rodent outbreaks: Ecology and impacts. International Rice Research Institute, Makati City

    Google Scholar 

  • Sorensen JS, Dearing MD (2003) Elimination of plant toxins by herbivorous woodrats: revisiting an explanation for dietary specialization in mammalian herbivores. Oecologia 134:88–94

    Article  CAS  PubMed  Google Scholar 

  • Sorensen JS, McLister JD, Dearing MD (2005) Plant secondary metabolites compromise the energy budgets of specialist and generalist mammalian herbivores. Ecology 86:125–139

    Article  Google Scholar 

  • Stapley J, Foley WJ, Cunningham R, Eschler B (2000) How well can common brushtail possums regulate their intake of Eucalyptus toxins? J Comp Physiol B Biochem Syst Environ Physiol 170:211–218

    Article  CAS  Google Scholar 

  • Stolter C, Ball JP, Julkunen-Tiitto R, Lieberei R, Ganzhorn JU (2005) Winter browsing of moose on two different willow species: food selection in relation to plant chemistry and plant response. J Zool 83:807–819

    CAS  Google Scholar 

  • Stolter C, Ball JP, Julkunen-Tiitto R (2013) Seasonal differences in the relative importance of specific phenolics and twig morphology result in contrasting patterns of foraging by a generalist herbivore. Can J Zool 91:338–347

    Article  CAS  Google Scholar 

  • Stowers L, Liberles SD (2016) State-dependent responses to sex pheromones in mouse. Curr Opin Neurobiol 38:74–79

    Article  CAS  PubMed  Google Scholar 

  • Takahashi A, Shimada T (2008) Selective consumption of acorns by the Japanese wood mouse according to tannin content: a behavioral countermeasure against plant secondary metabolites. Ecol Res 23:1033–1038

    Article  CAS  Google Scholar 

  • Thorp N (2011) Products Exempt from EPA Registration (Mammals). In: Toxipedia. http://www.toxipedia.org/pages/viewpage.action?pageId=6015109. Accessed 12 Jan 2016

  • Tiainen M, Pusenius J, Julkunen-Tiitto R, Roininen H (2006) Intraspecific competition, growth, chemistry, and susceptibility to voles in seedlings of Betula pendula. J Chem Ecol 32:2287–2301

    Article  CAS  PubMed  Google Scholar 

  • Torregrossa AM, Azzara AV, Dearing MD (2012) Testing the diet-breadth trade-off hypothesis: differential regulation of novel plant secondary compounds by a specialist and a generalist herbivore. Oecologia 168:711–718

    Article  PubMed  Google Scholar 

  • Tran TT, Hinds LA (2012) Fertility control of rodent pests: a review of the inhibitory effects of plant extracts on ovarian function. Pest Manag Sci 69:342–354

    Article  PubMed  CAS  Google Scholar 

  • Upadhyay RK, Ahmad S (2011) Management strategies for control of stored grain insect pests in farmer stores and public ware houses. World J Agric Sci 7:527–549

    Google Scholar 

  • Valchev I, Binev R, Yordanova V, Nikolov Y (2008) Anticoagulant rodenticide intoxication in animals - a review. Turkish. J Vet Anim Sci 32:237–243

    CAS  Google Scholar 

  • Van Cauwenberghe E, Maes L, Spittaels H, van Lenthe FJ, Brug J, Oppert J-M, De Bourdeaudhuij I (2010) Effectiveness of school-based interventions in Europe to promote healthy nutrition in children and adolescents: systematic review of published and “grey”literature. Br J Nutr 103:781–797

    Article  CAS  PubMed  Google Scholar 

  • Vehviläinen H, Koricheva J (2006) Moose and vole browsing patterns in experimentally assembled pure and mixed forest stands. Ecography 29:497–506

    Article  Google Scholar 

  • Virjamo V, Julkunen-Tiitto R, Henttonen H, Hiltunen E, Karjalainen R, Korhonen J, Huitu O (2013) Differences in vole preference, secondary chemistry and nutrient levels between naturally regenerated and planted Norway spruce seedlings. J Chem Ecol 39:1322–1334

    Article  CAS  PubMed  Google Scholar 

  • Wagner KK, Nolte DL (2001) Comparison of active ingredients and delivery systems in deer repellents. Wildl Soc Bull 29:322–330

    Google Scholar 

  • Watkins RW, Mosson HJ, Gurney JE, Cowan DP, Edwards JP (1996) Cinnamic acid derivatives: novel repellent seed dressings for the protection of wheat seed against damage by the field slug, Deroceras reticulatum. Crop Prot 15:77–83

    Article  CAS  Google Scholar 

  • Watkins RW, Gurney E, Cowan DP (1998) Taste-aversion conditioning of house mice (Mus domesticus) using the non-lethal repellent, cinnamamide. Appl Anim Behav Sci 57:171–177

    Article  Google Scholar 

  • Wiggins NL, McArthur C, McLean S, Boyle R (2003) Effects of two plant secondary metabolites, cineole and gallic acid, on nightly feeding patterns of the common brushtail possum. J Chem Ecol 29:1447–1464

    Article  CAS  PubMed  Google Scholar 

  • Willoughby IH, Jinks RL, Morgan GW, Pepper H, Budd J, Mayle B (2010) The use of repellents to reduce predation of tree seed by wood mice (Apodemus sylvaticus L.) and grey squirrels (Sciurus carolinensis Gmelin). Eur J For Res 130:601–611

    Article  CAS  Google Scholar 

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Acknowledgments

We thank Alexander Stuart for comments that improved an earlier draft of the manuscript. Part of this study was funded by a grant of Netafim Ltd., Israel.

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Authors and Affiliations

  1. Julius Kühn Institute, Federal Research Centre for Cultivated Plants, Institute for Plant Protection in Horticulture and Forests, Vertebrate Research, Münster, Germany

    Sabine C. Hansen, Christian Imholt & Jens Jacob

  2. University Hamburg, Biocenter Grindel and Zoological Museum, Hamburg, Germany

    Sabine C. Hansen & Caroline Stolter

Authors
  1. Sabine C. Hansen
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  2. Caroline Stolter
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  3. Christian Imholt
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  4. Jens Jacob
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Correspondence to Sabine C. Hansen.

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Hansen, S.C., Stolter, C., Imholt, C. et al. Plant Secondary Metabolites as Rodent Repellents: a Systematic Review. J Chem Ecol 42, 970–983 (2016). https://doi.org/10.1007/s10886-016-0760-5

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  • DOI: https://doi.org/10.1007/s10886-016-0760-5

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