Physiological and behavioural effects of fruit toxins on seed-predating versus seed-dispersing congeneric rodents

Journal of Experimental Biology

Volumn 216, Issue 19, 2013, Pages 3667-3673

  Samuni Blank, Michal ^a   Izhaki, Ido ^b   Dearing, M Denise ^c   Karasov, William H ^d   Gerchman, Yoram ^b   Kohl, Kevin D ^c   Lymberakis, Petros ^e   Kurnath, Patrice ^c   Arad, Zeev ^a  

^a TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^b UNIVERSITY OF HAIFA   (Israel)

^c UNIVERSITY OF UTAH   (United States)

^d UNIVERSITY OF WISCONSIN MADISON   (United States)

^e UNIVERSITY OF CRETE   (Greece)

Author keywords

Acomys; Alanine aminotransferase; Bitter taste; Body mass; Fruits; Glucosinolates; Liver; Pulp; Secondary compounds; Seeds

Indexed keywords

ALANINE AMINOTRANSFERASE; GLUCOSINOLATE; TOXIN;

ACOMYS; ANIMAL; ARTICLE; BITTER TASTE; BLOOD; BODY MASS; BODY SIZE; CHEMISTRY; EATING; ECOSYSTEM; ENZYMOLOGY; FEEDING BEHAVIOR; FRUIT; FRUITS; HYDROLYSIS; LIVER; METABOLISM; MURINAE; PHYSIOLOGY; PLANT SEED; PULP; RESEDACEAE; SECONDARY COMPOUNDS; SEED DISPERSAL;

ACOMYS; ALANINE AMINOTRANSFERASE; BITTER TASTE; BODY MASS; FRUITS; GLUCOSINOLATES; LIVER; PULP; SECONDARY COMPOUNDS; SEEDS;

ALANINE TRANSAMINASE; ANIMALS; BODY SIZE; EATING; ECOSYSTEM; FEEDING BEHAVIOR; FRUIT; GLUCOSINOLATES; HYDROLYSIS; MURINAE; RESEDACEAE; SEED DISPERSAL; SEEDS; TOXINS, BIOLOGICAL;

EID: 84883587501     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.089664     Document Type: Article

References (53)

1. Barome, P. O., Lymberakis, P., Monnerot, M. and Gautun, J. C. (2001). Cytochrome b sequences reveal Acomys minous (Rodentia, Muridae) paraphyly and answer the question about the ancestral karyotype of Acomys dimidiatus. Mol. Phylogenet. Evol. 18, 37-46.
2. Bronstein, J. L., Izhaki, I., Nathan, R., Tewksbury, J. J., Spiegel, O., Lotan, A., Altstein, O., Dennis, A. J., Schupp, E. W. and Green, R. J. (2007). Fleshy-fruited plants and frugivores in desert ecosystems. In Seed Dispersal: Theory and its Application in a Changing World (ed. A. J. Dennis, E. W. Schupp, R. J. Green and D. W. Westcott), pp. 148-177. Wallingford: CAB International.
3. Chandrashekar, J., Mueller, K. L., Hoon, M. A., Adler, E., Feng, L., Guo, W., Zuker, C. S. and Ryba, N. J. P. (2000). T2Rs function as bitter taste receptors. Cell 100, 703-711.
4. Chandrashekar, J., Hoon, M. A., Ryba, N. J. and Zuker, C. S. (2006). The receptors and cells for mammalian taste. Nature 444, 288-294.
5. Cipollini, M. L. and Levey, D. J. (1997). Secondary metabolites of fleshy vertebratedispersed fruits: adaptive hypotheses and implications for seed dispersal. Am. Nat. 150, 346-372.
6. Corlett, R. T. and Lucas, P. W. (1990). Alternative seed-handling strategies in primates: seed-spitting by long-tailed macaques (Macaca fasicularis). Oecologia 82, 166-171.
7. Das, S., Tyagi, A. K. and Kaur, H. (2000). Cancer modulation by glucosinolates: a review. Curr. Sci. 79, 1665-1671.
8. Dearing, M. D., Foley, W. J. and 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.
9. Dominy, N. J. and Duncan, B. W. (2005). Seed-spitting primates and the conservation and dispersion of large-seeded trees. Int. J. Primatol. 26, 631-649.
10. Duncan, A. J. and Milne, J. A. (1992). Effect of long-term intra-ruminal infusion of the glucosinolate metabolite allyl cyanide on the voluntary food intake and metabolism of lambs. J. Sci. Food Agric. 58, 9-14.
11. Duncan, A. J. and Milne, J. A. (1993). Effects of oral administration of brassica secondary metabolites, allyl cyanide, allyl isothiocyanate and dimethyl disulphide, on the voluntary food intake and metabolism of sheep. Br. J. Nutr. 70, 631-645.
12. Ehrhardt, N., Heldmaier, G. and Exner, C. (2005). Adaptive mechanisms during food restriction in Acomys russatus: the use of torpor for desert survival. J. Comp. Physiol. B 175, 193-200.
13. Fenwick, G. R., Heaney, R. K. and Mullin, W. J. (1983a). Bitterness in Brussels sprouts (Brassica oleracea L. var. gemnifera): the role of glucosinolates and their breakdown products. J. Sci. Food Agric. 34, 73-80.
14. Fenwick, G. R., Heaney, R. K. and Mullin, W. J. (1983b). Glucosinolates and their breakdown products in food and food plants. Crit. Rev. Food Sci. Nutr. 18, 123-201.
15. Garcia-Bailo, B., Toguri, C., Eny, K. M. and El-Sohemy, A. (2009). Genetic variation in taste and its influence on food selection. OMICS 13, 69-80.
16. Gautier-Hion, A., Gautier, J.-P. and Maisels, F. (1993). Seed dispersal versus seed predation: an inter-site comparison of two related African monkeys. Vegetatio 108, 237-244.
17. Glendinning, J. I., Brower, L. P. and Montgomery, C. A. (1990). Responses of three mouse species to deterrent chemicals in the monarch butterfly. I. Taste and toxicity tests using artificial diets laced with digitoxin or monocrotaline. Chemoecol. 1, 114- 123.
18. Gutman, R., Choshniak, I. and Kronfeld-Schor, N. (2006). Defending body mass during food restriction in Acomys russatus: a desert rodent that does not store food. Am. J. Physiol. 290, R881-R891.
19. Haim, A. and Borut, A. (1981). Heat production and dissipation in golden spiny mice, Acomys russatus, from two extreme habitats. J. Comp. Physiol. B 142, 445-450.
20. Haim, A., Yedidia, I., Haim, D. and Zisapel, N. (1994). Photoperiodicity in daily rhythms of body temperature, food and energy intake of the golden spiny mouse (Acomys russatus). Isr. J. Zool. 40, 145-150.
21. Haim, A., Alma, A. and Neuman, A. (2005). Body mass is a thermoregulatory adaptation of diurnal rodents to the desert environment. J. Therm. Biol. 31, 168-171.
22. Herrera, C. M. (1982). Defense of ripe fruit from pests: its significance in relation to plant-disperser interactions. Am. Nat. 120, 218-241.
23. Hopkins, R. J., van Dam, N. M. and van Loon, J. J. (2009). Role of glucosinolates in insect-plant relationships and multitrophic interactions. Annu. Rev. Entomol. 54, 57- 83.
24. Hyder, M. A., Hasan, M. and Mohieldein, A. H. (2013). Comparative levels of ALT, AST, ALP and GGT in liver associated diseases. Eur. J. Exp. Biol. 3, 280-284.
25. Izhaki, I. (2002a). Emodin - a secondary metabolite with multiple ecological functions in higher plants (a review). New Phytol. 155, 205-217.
26. Izhaki, I. (2002b). The role of fruit traits in determining fruit removal in east Mediterranean ecosystems. In Seed Dispersal and Frugivory: Ecology, Evolution and Conservation (ed. D. J. Levey, W. R. Silva and M. Galetti), pp. 161-175. Wallingford: CAB International.
27. Jordano, P. (2000). Fruit and frugivory. In Seeds: The Ecology of Regeneration in Plant Communities, 2nd edn (ed. M. Fenner), pp. 125-166. Wallingford: CAB International.
28. Kam, M. and Degen, A. A. (1993). Effect of dietary performed water on energy and water budgets of two sympatric desert rodents, Acomys russatus and Acomys cahirinus. J. Zool. 231, 51-59.
29. Kaplin, B. A. and Moermond, T. C. (1998). Variation in seed handling by two species of forest monkeys in Rwanda. Am. J. Primatol. 45, 83-101.
30. Kelt, D. A., Meserve, P. L. and Gutiérrez, J. R. (2004). Seed removal by small mammals, birds and ants in semi arid Chile, and comparison with other systems. J. Biogeogr. 31, 931-942.
31. Kim, D. J., Han, B. S., Ahn, B., Hasegawa, R., Shirai, T., Ito, N. and Tsuda, H. (1997). Enhancement by indole-3-carbinol of liver and thyroid gland neoplastic development in a rat medium-term multiorgan carcinogenesis model. Carcinogenesis 18, 377-381.
32. Kjaer, A. (1976). Glucosinolates in the Cruciferae. In The Biology and Chemistry of the Cruciferae (ed. J. G. Vaughan, A. J. Macleod and B. M. G. Jones), pp. 207-219. London: Academic Press.
33. Lambert, J. E. (1999). Seed handling in chimpanzees (Pan troglodytes) and redtail monkeys (Cercopithecus ascanius): implications for understanding hominoid and cercopithecine fruit-processing strategies and seed dispersal. Am. J. Phys. Anthropol. 109, 365-386.
34. Levey, D. J. (1987). Seed size and fruit-handling techniques of avian frugivores. Am. Nat. 129, 471-485.
35. Levy, O., Dayan, T. and Kronfeld-Schor, N. (2011). Interspecific competition and torpor in golden spiny mice: two sides of the energy-acquisition coin. Integr. Comp. Biol. 51, 441-448.
36. McArthur, C., Hagerman, A. E. and Robbins, C. T. (1991). Physiological strategies of mammalian herbivores against plant defenses. In Plant Defenses Against Mammalian Herbivory (ed. R. T. Palo and C. T. Robbins), pp. 103-114. Boca Raton, FL: CRC Press.
37. Mueller, K. L., Hoon, M. A., Erlenbach, I., Chandrashekar, J., Zuker, C. S. and Ryba, N. J. P. (2005). The receptors and coding logic for bitter taste. Nature 434, 225-229.
38. Nelson, G., Hoon, M. A., Chandrashekar, J., Zhang, Y., Ryba, N. J. P. and Zuker, C. S. (2001). Mammalian sweet taste receptors. Cell 106, 381-390.
39. Ozer, J., Ratner, M., Shaw, M., Bailey, W. and Schomaker, S. (2008). The current state of serum biomarkers of hepatotoxicity. Toxicology 245, 194-205.
40. Rask, L., Andréasson, E., Ekbom, B., Eriksson, S., Pontoppidan, B. and Meijer, J. (2000). Myrosinase: gene family evolution and herbivore defense in Brassicaceae. Plant Mol. Biol. 42, 93-114.
41. Salt, W. B., II (2004). Nonalcoholic fatty liver disease (NAFLD): a comprehensive review. J. Insur. Med. 36, 27-41.
42. Samuni-Blank, M., Izhaki, I., Dearing, M. D., Gerchman, Y., Trabelcy, B., Lotan, A., Karasov, W. H. and Arad, Z. (2012). Intraspecific directed deterrence by the mustard oil bomb in a desert plant. Curr. Biol. 22, 1218-1220.
43. Samuni-Blank, M., Arad, Z., Dearing, M. D., Gerchman, Y., Karasov, W. H. and Izhaki, I. (2013). Friend or foe? Disparate plant-animal interactions of two congeneric rodents. Evol. Ecol. doi:10.1007/s10682-013-9655-x
44. Scalera, G. (1992). Taste preferences, body weight gain, food and fluid intake in singly or group-housed rats. Physiol. Behav. 52, 935-943.
45. Shkolnik, A. and Borut, A. (1969). Temperature and water relations in two species of spiny mice (Acomys). J. Mammal. 50, 245-255.
46. Sørensen, M., Jensen, B. R., Poulsen, H. E., Deng, X., Tygstrup, N., Dalhoff, K. and Loft, S. (2001). Effects of a Brussels sprouts extract on oxidative DNA damage and metabolising enzymes in rat liver. Food Chem. Toxicol. 39, 533-540.
47. Sorensen, J. S., McLister, J. D. and Dearing, M. D. (2005). Plant secondary metabolites compromise the energy budget of specialist and generalist mammalian herbivores. Ecology 86, 125-139.
48. Spiegel, O. and Nathan, R. (2007). Incorporating dispersal distance into the disperser effectiveness framework: frugivorous birds provide complementary dispersal to plants in a patchy environment. Ecol. Lett. 10, 718-728.
49. Spiegel, O. and Nathan, R. (2011). Empirical evaluation of directed dispersal and density-dependent effects across successive recruitment phases. J. Ecol. 100, 392- 404.
50. Torregrossa, A. M., Azzara, A. V. and Dearing, M. D. (2011). Differential regulation of plant secondary compounds by herbivorous rodents. Funct. Ecol. 25, 1232-1240.
51. Volobouev, V., Auffray, J. C., Debat, V., Denys, C., Gautun, J. C. and Tranier, M. (2007). Species delimitation in the Acomys cahirinus - dimidiatus complex (Rodentia, Muridae) inferred from chromosomal and morphological analyses. Biol. J. Linn. Soc. Lond. 91, 203-214.
52. Wang, X., Cao, Y., Fu, Y., Guo, G. and Zhang, X. (2011). Liver fatty acid composition in mice with or without nonalcoholic fatty liver disease. Lipids Health Dis. 10, 234.
53. Wittstock, U. and Halkier, B. A. (2002). Glucosinolate research in the Arabidopsis era. Trends Plant Sci. 7, 263-270.