Coevolution of Cyanogenic Bamboos and Bamboo Lemurs on Madagascar

PLoS ONE

Volumn 11, Issue 8, 2016, Pages

  Ballhorn, Daniel J ^a   Rakotoarivelo, Fanny Patrika ^b   Kautz, Stefanie ^a  

^a PORTLAND STATE UNIVERSITY   (United States)

^b UNIVERSITÉ DE LA RÉUNION   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CYANIDE; PROTEIN;

ADAPTIVE RADIATION; ARTICLE; BAMBOO; BAMBUSA MADAGASCARIENSIS; CATHARIOSTACHYS CAPITATA; CATHARIOSTACHYS MADAGASCARIENSIS; CEPHALOSTACHYUM; COEVOLUTION; CYANOGENESIS; EVOLUTIONARY ADAPTATION; FOOD CROP; FOOD QUALITY; FORAGING; HOST RANGE; LEMURIDAE; MADAGASCAR; MOLECULAR PHYLOGENY; NASTUS ELONGATUS; NONHUMAN; PROLEMUR SIMUS; SYMPATRY; ANIMAL; BAMBUSA; CHEMISTRY; DIET; EVOLUTION; FEEDING BEHAVIOR; METABOLISM; PHYLOGENY; SEQUENCE ALIGNMENT;

ANIMALS; BAMBUSA; BIOLOGICAL EVOLUTION; CYANIDES; DIET; FEEDING BEHAVIOR; LEMUR; MADAGASCAR; PHYLOGENY; SEQUENCE ALIGNMENT;

EID: 84984922319     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0158935     Document Type: Article

References (141)

1. Berenbaum M, Feeny P (1981) Toxicity of angular furanocoumarins to swallowtail butterflies-escalation in a co-evolutionary arms-race. Science 212:927-929.
2. Kareiva P (1999) Coevolutionary arms races: Is victory possible? Proc Nat Acad Sci USA 96:8-10.
3. Thompson JN (1994) The Coevolutionary Process. University of Chicago Press, Chicago, USA.
4. Bernays E, Graham M (1988) On the evolution of host specificity in phytophagous arthropods. Ecology 69:886-892.
5. Berenbaum MR, Zangerl AR (1998) Chemical phenotype matching between a plant and its insect herbivore. Proc Nat Acad Sci USA 95:13743-13748.
6. Haley SL, Lamb JG, Franklin MR, Constance JE, Dearing MD (2007) Xenobiotic metabolism of plant secondary compounds in juniper (Juniperus monosperma) by specialist and generalist woodrat herbivores, genus Neotoma. Comp Biochem Physiol. C-Toxicol Pharmacol 146:552-560.
7. Johansson J, Bergström A, Janz N (2007) The benefit of additional oviposition targets for a polyphageous butterfly. J Insect Sci 7:1-9.
8. Li W, Schuler MA, Berenbaum MR (2003) Diversification of furanocoumarin-metabolizing cytochrome P450 monoxygenase in two papilionids: specificity and substrate encounter rate. Proc Natl Acad Sci USA 100:14593-14598.
9. Freeland WJ, Janzen DH (1974) Strategies in herbivory by mammals: The role of plant secondary compounds. Am Nat 108:269-289.
10. Guglielmo CG, Karasov WH, Jakubas WJ (1996) Nutritional costs of a plant secondary metabolite explain selective foraging by ruffed grouse. Ecology 77:1103-1115.
11. Bernays EA, Minkenberg O (1997) Insect herbivores: Different reasons for being a generalist. Ecology 78:1157-1169.
12. Ehrlich PR, Raven PH (1964) Butterflies and plants-A study in coevolution. Evolution 18:586-608.
13. Janzen DH (1980) When is it coevolution? Evolution 34:611-612.
14. Jaenike J (1990) Host specialization in phytophageous insects. Ann Rev Ecol Syst 21:243-273.
15. Rasmann S, Agrawal AA (2011) Evolution of specialization: A phylogenetic study of host range in the red milkweed beetle (Tetraopes tetraophthalmus). Am Nat 177:728-737. doi: 10.1086/659948
16. Evans LM, Allan GJ, Shuster SM, Woolbright SA, Whitham TG (2008) Tree hybridization and genotypic variation drive cryptic speciation of a specialist mite herbivore. Evolution 62:3027-3040. doi: 10. 1111/j.1558-5646.2008.00497.x
17. Mason JR, Maruniak JA (1983) Behavioral and physiological effects of capsaicin in redwinged blackbirds. Pharmacol. Biochem. Behav. 19: 857-862.
18. Bryant JP, Clausen TP, Swihart RK, Landhausser SM, Stevens MT, Hawkins CD, et al. (2009) Fire drives transcontinental variation in tree birch defense against browsing by snowshoe hares. Am Nat 174:13-23. doi: 10.1086/599304
19. DeGabriel JL, Moore BD, Foley WJ, Johnson CN (2009) The effects of plant defensive chemistry on nutrient availability predict reproductive success in a mammal. Ecology 90:711-719.
20. Feng ZL, Liu RS, DeAngelis DL, Bryant JP, Kielland K, Chapin FS III, et al. (2009) Plant toxicity, adaptive herbivory, and plant community dynamics. Ecosystems 12:534-547.
21. Carmona D, Lajeunesse MJ, Johnson MTJ (2011) Plant traits that predict resistance to herbivores. Func Ecol 25:358-367.
22. Skopec MM, Dearing MD (2011) Differential expression and activity of catechol-Omethyl transferase (COMT) in a generalist (Neotoma albigula) and juniper specialist (Neotoma stephensi) woodrat. Comp Biochem Physiol C-Toxicol Pharmacol 154:383-390. doi: 10.1016/j.cbpc.2011.07.010
23. Crawley MJ (1983) Studies in ecology. Vol. 10. Oxford: Blackwell Scientific Publications; Herbivory: The dynamics of animal-plant interactions.
24. Bernays EA, Chapman RG (1994) Host-plant selection by phytophagous insects. New York: Chapman & Hall.
25. Lawler IR, Foley WJ, Eschler BM, Pass DM, Handasyde K (1998) Interspecific variation in Eucalyptus secondary metabolites determines food intake by folivorous marsupials. Oecologia 116:160-169.
26. Boyle RT, McLean S, Davies N, Foley W, Moore B. (1999) Folivorous specialization: Adaptations in the detoxification of the dietary terpene, p-cymene, in Australian marsupial folivores. Am Zool 39:120A.
27. Dearing MD, Mangione AM, Karasov WH (2000) Diet breadth of mammalian herbivores: nutrient vs. detoxification constraints. Oecologia 123:397-405.
28. Marsh KJ, Wallis IJ, Foley WJ (2003) The effect of inactivating tannins on the intake of Eucalyptus foliage by a specialist Eucalyptus folivore Pseudocheirus peregrines and a generalist herbivore Trichosurus vulpecula. Aust J Zool 51:31-42.
29. Sorensen JS, Dearing MD (2003) Elimination of plant toxins by herbivorous woodrats: revisiting an explanation for dietary specialization in mammalian herbivores. Oecologia 134:188-94.
30. Shipley LA, Davila TB, Thines NJ, Elias BA (2006) Nutritional requirements and diet choices of the pygmy rabbit (Brachylagus idahoensis): A sagebrush specialist. J Chem Ecol 32:2455-2474.
31. Dearing MD, Cork S (1999) Role of detoxification of plant secondary compounds on diet breadth in a mammalian herbivore, Trichosurus vulpecula. J Chem Ecol 25:1205-1219.
32. Sorensen JS, Heward E, Dearing MD (2005a) Plant secondary metabolites alter the feeding patterns of a mammalian herbivore (Neotoma lepida). Oecologia 146:415-422.
33. Wiggins NL, McArthur C, Davies NW (2006a) Diet switching in a generalist mammalian folivore: fundamental to maximising intake. Oecologia 147:650-657.
34. Ali JG, Agrawal AA (2012) Specialist versus generalist insect herbivores and plant defense. Trends Plant Sci 17:293-302. doi: 10.1016/j.tplants.2012.02.006
35. Engler HS, Spencer KC, Gilbert LE (2000) Insect metabolism: preventing cyanide release from leaves. Nature 406: 144-145
36. Pentzold S, Zagrobelny M, Roelsgaard PS, Møller BL, Bak S (2014) The multiple strategies of an insect herbivore to overcome plant cyanogenic glucoside defence. PLoS ONE 9(3): e91337. doi: 10. 1371/journal.pone.0091337
37. Robinson BW, Wilson DS (1998) Optimal foraging, specialization, and a solution to Liem's Paradox. Am Nat 151:223-35. doi: 10.1086/286113
38. McArthur C, Hagerman AE, Robbins CT (1991) Physiological strategies of mammalian herbivores against plant defenses. In: Palo R.T., Robbins C.T., editors. Plant defenses against mammalian herbivory. Boca Raton, Florida: CRC Press; p. 103-114.
39. Shipley LA, Forbey JS, Moore BD (2009) Revisiting the dietary niche: When is a mammalian herbivore a specialist? Int Comp Biol 49: 274-290.
40. Tan CL (1999) Group composition, home range size, and diet of three sympatric bamboo lemur species (Genus Hapalemur) in Ranomafana National Park, Madagascar. Int J Primatol 20:547-566.
41. Wright PC, Johnson SE, Irwin MT, Jacobs R, Schlichting P, Lehman S, et al. (2008) The crisis of the critically endangered Greater Bamboo Lemur (Prolemur simus). Prim Conserv 23:5-17.
42. Eppley TM, Verjans E, Donati G (2011) Coping with low-quality diets: A first account of the feeding ecology of the southern gentle lemur, Hapalemur meridionalis, in the Mandena littoral forest, southeast Madagascar. Primates 52:7-13. doi: 10.1007/s10329-010-0225-3
43. Meier B, Albignac R, Peyrieras A, Rumpler Y, Wright P (1987) A new species of Hapalemur (Primates) from south east Madagascar. Folia Primatol 48:211-215.
44. Glander KE, Wright PC, Seigler DS, Radrianasolo V, Randrianasolo B (1989) Consumption of cyanogenic bamboo by a newly discovered species of bamboo lemur. Am J Primatol 19:119-124.
45. Wright PC, Randriamanantena M (1989) Behavioral ecology of three sympatric bamboo lemurs in Madagascar. Am J Phys Anthropol 788:327.
46. Overdorff DJ, Strait SG, Telo A (1997) Seasonal variation in activity and diet in a small-bodied folivorous primate, Hapalemur griseus, in Southeastern Madagascar. Am J Primatol 43:211-223.
47. Mittermeier R, Ganzhorn JU, Konstant W, Glander K, Tattersall I, Groves CP, et al. (2008) Lemur diversity in Madagascar. Int J Primatol 29:1607-1656.
48. Ballhorn DJ, Kautz S, Rakotoarivelo FP (2009) Quantitative variability of cyanogenesis in Cathariostachys madagascariensis-The main food plant of bamboo lemurs in Southeastern Madagascar. Am J Primatol 71:305-315. doi: 10.1002/ajp.20653
49. Ballhorn DJ, Kautz S, Jensen M, Schmitt I, Heil M, Hegeman AD (2011) Genetic and environmental interactions determine plant defences against herbivores. J Ecol 99: 313-326.
50. Solomonson LP (1981) Cyanide is a metabolic inhbitor in B. Vennesland, Conn E. E., Knowles C. J., Westby J. and Wiising F., eds. Cyanide in Biology. Academic Press, London, UK.
51. Dirzo R, Harper JL (1982) Experimental studies on slug-plant interactions IV. The performance of cyanogenic and acyanogenic morphs of Trifolium repens in the field. J Ecol 70:119-138.
52. Zentek J (1997) Case report: Bloat and diarrhoea in calves. Deutsche Tierarztliche Wochenschrift 104:153-155.
53. Banea-Mayambu JP, Tylleskar T, Tylleskar K, Gebre-Medhin M, Rosling H (2000) Dietary cyanide from insufficiently processed cassava and growth retardation in children in the Democratic Republic of Congo (formerly Zaire). Ann Trop Paediatr 20:34-40.
54. Magalhaes CP, Xavier J, Campos AP (2000) Biochemical basis of the toxicity of manipueira (liquid extract of cassava roots) to nematodes and insects. Phytochem Anal 11:57-60.
55. Brown JH (1984) On the relationship between abundance and distribution of species. Am Nat 124:255-279.
56. Braby MF (2012) The taxonomy and ecology of Delias aestiva Butler, 1897 stat. rev. (Lepidoptera: Pieridae), a unique mangrove specialist of Euphorbiaceae from northern Australia. Biol J Linn Soc, 107:697-720.
57. Goodman SM, Razafindratsita V, Schötz H, Ratsimbazafy R (2001) Les lémuriens. In: Inventaire Biologique du Parc National de Ranomafana et du Couloir Forestier qui la Relie au Parc National d'Andringitra, Goodman S. M. and Razafindratsita V. (eds.), pp.231-243. CIDST, Antananarivo, Madagascar.
58. Rakotondravony D, Razafindramahatra LV (2004) Contribution á l'étude des populations de Hapalemur aureus dans le couloir forestier Ranomafana-Andringitra. Lemur News 9:28-32.
59. Lehman SM, Wright PC (2000) Preliminary study of the conservation status of lemur communities Betsakafandrika region of eastern Madagascar. Lemur News 5:23-25.
60. Mittermeier RA, Konstant WR, Nicoll ME, Langrand O (1992) Lemurs of Madagascar: An action plan for their conservation 1993-1999. IUCN, Gland, Switzerland.
61. Mittermeier RA, Tattersall I, Konstant WR, Meyers DM, Mast RB (1994) Lemurs of palearctic Anthidiine bees Madagascar. Conserv Intl., Washington DC, USA.
62. Dolch R, Fiely JL, Ndriamiary J-N, Rafalimandimby J, Randriamampionona R, Engberg SE, et al. (2008) Confirmation of the greater bamboo lemur, Prolemur simus, north of the Torotorofotsy wetlands, eastern Madagascar. Lemur News 13:14-17.
63. Dolch R, Hilgartner RD, Ndriamiary JN, Randriamahazo H (2004) The grandmother of all bamboo lemurs: evidence for the occurrence of Hapalemur simus in fragmented rainforest surrounding the Torotorofotsy marshes, central eastern Madagascar. Lemur News 9:24-26.
64. Rakotosamimanana B, Ralaiarison RR, Ralisoamalala RC, Rasolofoharivelo TM, Raharimanantsoa V, Randrianarison M, et al. (2004) Comment et pourquoi les lémuriens diurnes disparaissent peu à peu dans les forêts d'Ambato et de Moramanga (région de Moramanga) Madagascar? Lemur News 9:19-24.
65. Godfrey LR, Vuillaume-Randriamanantena M (1986) Hapalemur simus: endangered lemur once widespread. Primate Conserv 7:92-96.
66. Tattersall I (1982) The primates of Madagascar. Columbia University Press, New York, USA.
67. Ganzhorn JU (1992) Leaf chemistry and the biomass of folivorous primates in tropical forests-Test of a hypothesis. Oecologia 91:540-547.
68. Ballhorn DJ, Heil M, Lieberei R (2006) Phenotypic plasticity of cyanogenesis in lima bean Phaseolus lunatus-Activity and activation of β-glucosidase. J Chem Ecol 32: 261-275.
69. Ballhorn DJ, Lieberei R, Ganzhorn JU (2005) Plant cyanogenesis of Phaseolus lunatus and its relevance for herbivore-plant interaction: The importance of quantitative data. J Chem Ecol 31:1445-1473.
70. Bradford MM (1976) Rapid and sensitive method for quantitation of microgram quantities of protein utilizing principle of protein-dye binding. Anal Biochem 72:248-254.
71. Rodriguez-Saona CR, Musser RO, Vogel H, Hum-Musser SM, Thaler JS (2010) Molecular, biochemical, and organismal analyses of tomato plants simultaneously attacked by herbivores from two feeding guilds. J Chem Ecol 36:1043-1057. doi: 10.1007/s10886-010-9854-7
72. Xin X, Jiang XM, Sun HM, YuWW(2007) Protein extraction from polyphenol-rich seeds of Quercus acutissima. Scientia Silvae Sinicae 43:26-30.
73. Isaacson T, Damasceno CMB, Saravanan RS, He Y, Catalá C, Saladié M, et al. (2006) Sample extraction techniques for enhanced proteomic analysis of plant tissues. Nat Prot 1:769-774.
74. Jordan WC, Courtney MW, Neigel JE (1996) Low levels of intraspecific genetic variation at a rapidly evolving chloroplast DNA locus in North American duckweeds (Lemnaceae). Am J Bot 83:430-439.
75. Kelchner SA, Clark LG (1997) Molecular evolution and phylogenetic utility of the chloroplast rpl16 intron in Chusquea and the Bambusoideae (Poaceae). Mol Phyl Evol 8:385-397.
76. Drummond A, Ashton B, Buxton S, Cheung M, Cooper A, Duran C, et al. (2011) Geneious v5.4, Available: http://www.geneious.com/.
77. Altschul SF, Madden TL, Schäffer AA (1997) Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucl. Acids Res. 25:3389-3402.
78. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucl Acids Res 32:1792-1797.
79. Kautz S, Lumbsch HT, Ward PS, Heil M (2009) How to prevent cheating: A digestive specialization ties mutualistic plant-Ants to their ant-plant partners. Evolution 63:839-853. doi: 10.1111/j.1558-5646.2008.00594.x
80. Huelsenbeck JP, Ronquist F (2001) MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 17:754-755.
81. Nylander JAA (2004) MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University.
82. Zwickl DJ (2006) Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. The University of Texas at Austin, Austin, USA.
83. Chatterjee HJ, Ho SYW, Barnes I, Groves C (2009) Estimating the phylogeny and divergence times of primates using a supermatrix approach. BMC Evol Biol 9:259. doi: 10.1186/1471-2148-9-259
84. Talavera G, Castresana J (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 56:564-577.
85. Nylander JAA, Ronquist F, Huelsenbeck JP, Nieves-Aldrey JL (2004) Bayesian phylogenetic analysis of combined data. Syst Biol 53:47-67.
86. Swofford DL (2002) Phylogenetic Analysis Using Parsimony. (and Other Methods). Version 4. Sinauer Associates, Sunderland, USA.
87. Felsenstein J (1985) Confidence limits on phylogenies: An approach using the bootstrap. Evolution 39:783-791.
88. Hillis DM, Bull JJ (1993) An empirical-Test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Systematic Biology 42:182-192.
89. Page RDM (1996) Treeview: An application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357-358.
90. Pagel M (1994) Detecting correlated evolution on phylogenies: A general method for the comparative analysis of discrete characters. Proc R Soc Biol Sci Ser B 255:37-45.
91. Maddison WP, Maddison DR (2007) Mesquite: A modular system for evolutionary analysis. Version 2.01.
92. Edwards AWF (1972) Likelihood. Cambridge University Press, Cambridge, USA.
93. Clark L, Dransfield S, Triplett J, Sánches-Ken J (2007) Phylogenetic relationships among the oneflowered, determinate genera of Bambuseae (Poaceae: Bambusoideae). Aliso 23:315-332.
94. Berenbaum M (1990) Evolution of specializaion in insect-umbellifer associations. Ann Rev Entomol 35:319-343.
95. Sorensen JS, Dearing MD (2006) Efflux transporters as a novel herbivore counter mechanism to plant chemical defenses. J Chem Ecol 32:1181-96.
96. Jakubas WJ, Karasov WH, Guglielmo CG (1993) Coniferyl benzoate in quaking aspen (Populus tremuloides)-its effect on energy and nitrogen digestion and retention in ruffed grouse (Bonasa umbellus). Physiol Zool 66:580-601.
97. Marsh KJ, Wallis IR, McLean S, Sorensen JS, Foley WJ (2006) Conflicting demands on detoxification pathways influence how common brushtail possums choose their diets. Ecology 87:2103-2112.
98. Sorensen JS, McLister JD, Dearing MD (2005b) Plant secondary metabolites compromise the energy budgets of specialist and generalist mammalian herbivores. Ecology 86:125-139.
99. Van der Meiden E (1996) Plant defence, an evolutionary dilemma: Contrasting effects of (specialist and generalist) herbivores and natural enemies. Entomol Exp Appl 80:307-310.
100. Ballhorn DJ, Heil M, Pietrowski A, Lieberei R (2007) Quantitative effects of cyanogenesis on an adapted herbivore. J Chem Ecol 33:2195-2208.
101. Ballhorn DJ, Kautz S, Lieberei R (2010) Comparing responses of generalist and specialist herbivores to various cyanogenic plant features. Entomol Exp Appl 134:245-259.
102. ZhangW(2000) Phylogeny of the grass family (Poaceae) from rpl16 intron sequence data. Mol Phyl Evol 15:135-146.
103. Gleadow RM, Woodrow IE (2000) Polymorphism in cyanogenic glycoside content and cyanogenic beta-glucosidase activity in natural populations of Eucalyptus cladocalyx. Australian J Plant Physio. 27:693-699.
104. Ballhorn DJ, . Kautz S, Lion U, Heil M (2008) Trade-offs between direct and indirect defences of lima bean (Phaseolus lunatus). J Ecol 96:971-980.
105. Cooper SM, Owensmith N, Bryant JP (1988) Foliage acceptability to browsing ruminants in relation to seasonal changes in the leaf chemistry of woody plants in a South African savanna. Oecologia 75:336-342.
106. Belovsky GE, Schmitz OJ (1994) Plant defenses and optimal foraging by mammalian herbivores. J Mammal 75:816-832.
107. Robbins C (1993) Wildlife feeding and nutrition. Academic Press, San Diego, C.A, USA.
108. Ball JP, Danell K, Sunesson P (2000) Response of a herbivore community to increased food quality and quantity: An experiment with nitrogen fertilizer in a boreal forest. J. Appl. Ecol. 37:247-255.
109. Montgomery RD (1969) Cyanogens. In: Liener IE, editor. Toxic constituents of plant foodstuffs. Academic Press, New York, USA.
110. Nahrstedt A (1985) Cyanogenic compounds as protecting agents for organisms. Plant Syst Evol 150:35-47.
111. Yamashita N, Tan CL, Vinyard CJ, Williams C. (2010). Semi-quantitative tests of cyanide in foods and excreta of three Hapalemur species in Madagascar. Am J Primatol 72:56-61. doi: 10.1002/ajp.20751
112. Schaller G, Jinchu H, Wenshi P, Jing Z (1985) Giant pandas of Wolong. University of Chicago Press, Chicago, IL, USA.
113. McKinney ML (1997) Extinction vulnerability and selectivity: Combining Ecological and Paleontological Views. Annu Rev Ecol Syst 28: 495-516.
114. Julliard R, Jiguet F, Couvet D (2004) Common birds facing global changes: what makes a species at risk? Glob Change Biol 10:148-154.
115. Biesmeijer JC, Roberts SPM, Reemer M, Ohlemöller R, Edwards M, Peeters T, et al. (2006) Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 313 (5785): 351-354
116. Futuyma DJ, Moreno G (1988) The evolution of ecological specialization. Ann Rev Ecol Syst 19:207-233.
117. Brooks DR, McLennan DA (2002) The Nature of Diversity. University of Chicago Press, Chicago, USA.
118. Stephens PR, Wiens JJ (2003) Ecological diversification and phylogeny of emydid turtles. Biol J Linn Soc 79:577-610.
119. Colles A, Liow LH, Prinzing A (2009) Are specialists at risk under environmental change? Neoecological, paleoecological and phylogenetic approaches. Ecol Lett 12:849-863. doi: 10.1111/j.1461-0248. 2009.01336.x
120. Lanyon SM (1992) Interspecific brood parasitism in blackbirds (Icterinae)-A phylogenetic perspective. Science 255:77-79.
121. Muller A (1996) Host-plant specialization in western (Hymenoptera: Apoidea: Megachilidae). Ecol Monogr 66:235-257.
122. Ballhorn DJ, Lieberei R (2006) Oviposition choice of Mexican bean beetle (Epilachna varivestis) depends on host plants cyanogenic capacity. J Chem Ecol 32:1861-1865.
123. Lobel PS, Ogden JC (1981) Foraging by the herbivorous parrotfish Sparisoma radians. Mar Biol 64:173-183.
124. Belovsky GE (1984a) Herbivore optimal foraging-A comparative test of 3 models. Am Nat 124:97-115.
125. Belovsky GE (1984b) Snowshoe hare optimal foraging and its implications for population dynamics. Theor Pop Biol 25:235-264.
126. Chung TK, Baker DH (1991) A chemically defined diet for maximal growth of pigs. J Nutr 121:979-984.
127. Leeson S, Caston LJ (1991) Response of 2 strains of turkey hens to various protein and energy feeding programs. Poul Sci 70:1739-1747.
128. Dearing MD, Schall JJ (1992) Testing models of optimal diet assembly by the generalist herbivorous lizard Cnemidophorus murinus. Ecology 73:845-858.
129. 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.
130. Wiggins NL, McArthur C, Davies NW, McLean S (2006b) Behavioral responses of a generalist mammalian folivore to the physiological constraints of a chemically defended diet. J Chem Ecol 32:1133-1147.
131. Villalba JJ, Provenza FD, Han GD (2004) Experience influences diet mixing by herbivores: implications for plant biochemical diversity. Oikos 107:100-109.
132. Papachristou TG, Dziba LE, Villalba JJ, Provenza FD (2007) Patterns of diet mixing by sheep offered foods varying in nutrients and plant secondary compounds. Appl Animal Beh Sci 108:68-80.
133. Garshelis DL, Wang H, Wang DJ, Zhu XJ, Li S, McShea WJ (2008) Do revised giant panda population estimates aid in their conservation? Ursus 19:168-176.
134. Li RQ, Fan W, Tian G, Zhu HM, He L, Cai J, et al. (2010) The sequence and de novo assembly of the giant panda genome. Nature 463:311-317. doi: 10.1038/nature08696
135. Martin RW, Handasyde KA (1999) The koala: natural history, conservation, and management. University of New South Wales Press and Krieger Publishing Company, Malabar, FL, USA.
136. Moore BD, Foley WJ (2000) A review of feeding and diet selection in koalas (Phascolarctos cinereus). Aust J Zool 48:317-333.
137. Bryant JP, Kuropat PJ (1980) Selection of winter forage by sub-Arctic browsing vertebrates-The role of plant chemistry. Ann. Rev. Ecol. Syst. 11:261-285.
138. Palo RT, Robbins CT (1991) Plant defenses against mammalian herbivory. CRC Press, Boca Raton, USA.
139. Pellmyr O, Thompson JN (1992) Multiple occurrences of mutualism in the yucca moth lineage. Proc Nat Acad Sci USA 89:2927-2929.
140. Novotny V, Drozd P, Miller SE, Kulfan M, Janda M, Basset Y, et al. (2006) Why are there so many species of herbivorous insects in tropical rainforests? Science 313:1115-1118.
141. Novotny V, Miller SE, Hulcr J, Drew RAI, Basset Y, Janda M, et al. (2007) Low beta diversity of herbivorous insects in tropical forests. Nature 448:692-695.