Feeding over the 24-h cycle: Dietary flexibility of cathemeral collared lemurs (Eulemur collaris)

Behavioral Ecology and Sociobiology

Volumn 61, Issue 8, 2007, Pages 1237-1251

  Donati, Giuseppe ^a   Bollen, An ^b   Borgognini Tarli, Silvana M ^a   Ganzhorn, Joerg U ^c  

^a UNIVERSITY OF PISA   (Italy)

^b UNEP   (Thailand)

^c UNIVERSITY OF HAMBURG   (Germany)

Author keywords

Cathemerality; Eulemur collaris; Feeding strategies; Lemur ecology; Nutritional intake

Indexed keywords

ADAPTATION; ANTIPREDATOR DEFENSE; AVOIDANCE REACTION; DIET; DIURNAL ACTIVITY; FEEDING BEHAVIOR; FOOD AVAILABILITY; FOREST ECOSYSTEM; NOCTURNAL ACTIVITY; NUTRIENT UPTAKE; PRIMATE;

ANIMALIA; AVES; EULEMUR FULVUS COLLARIS; LEMUR; LEMURIDAE; MAMMALIA; RAPTORES; STREPSIRHINI;

EID: 34248393406     PISSN: 03405443     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00265-007-0354-x     Document Type: Article

References (111)

1. Altmann J (1974) Observational study of behaviour: sampling methods. Behaviour 49:227-267
2. Andrews J, Birkinshaw C (1998) A comparison between the daytime and night-time diet, activity and feeding height of the black lemur, Eulemur macaco (Primates: Lemuridae), in Lokobe Forest, Madagascar. Folia Primatol 69:175-182
3. Aschoff J, Daan S, Groos GA (1982) Vertebrate circadian systems. Springer, Berlin
4. Bollen A, Donati G (2005) Phenology of the littoral forest of Sainte Luce, south-east Madagascar. Biotropica 37:32-43
5. Bollen A, Donati G, Fietz J, Schwab D, Ramanamanjato J-B, Randrihasipara L, Elsacker L van, Ganzhorn JU (2005) Fruit characteristics in a dry deciduous and a humid littoral forest of Madagascar: evidence for selection pressure through abiotic constraints rather than through coevolution by seed dispersers. In: Dew L, Boubli JP (eds) Tropical fruits and frugivores: the search for strong interactors. Kluwer, MA, pp 92-118
6. Campbell JL, Williams CV, Eisemann JH (2004) Use of total dietary fiber across four lemur species (Propithecus verreauxi coquereli, Hapalemur griseus griseus, Varecia variegata, and Eulemur fulvus): does fiber type affect digestive efficiency? Am J Primatol 64:323-335
7. Charles-Dominique P (1975) Nocturnality and diurnality: an ecological interpretation of these two modes of life by an analysis of the higher vertebrate fauna in tropical forest ecosystems. In: Luckett WP, Szalay FS (eds) Phylogeny of the primates. Plenum, New York, pp 69-88
8. Chiarello AG (1998) Activity budgets and ranging patterns of the Atlantic forest maned sloth Bradypus torquatus (Xenarthra: Bradypodidae). J Zool 246:1-10
9. Chivers DJ (1995) Functional anatomy of the gastrointestinal tract. In: Davies AG, Oates JF (eds) Colobine monkeys. Cambridge University Press, Cambridge, pp 205-226
10. Chivers DJ, Hladik CM (1980) Morphology of the gastrointestinal tract in primates: comparisons with other mammals in relation to diet. J Morphol 166:337-386
11. Colquhoun IC (1998) Cathemeral behaviour of Eulemur macaco macaco at Ambato Massif, Madagascar. Folia Primatol 69:22-34
12. Colquhoun IC (2006) Predation and cathemerality. Folia Primatol 77:143-165
13. Cork SJ, Foley WJ (1991) Digestive and metabolic strategies of arboreal mammalian folivores in relation to chemical defenses in temperate and tropical forests. In: Palo RH, Robbins CT (eds) Plants defenses against mammalian herbivory. CRC, Boca Raton, Florida, pp 133-165
14. Curtis DJ, Rasmussen MA (2002) Cathemerality in lemurs. Evol Anthropol 11(Suppl):83-86
15. Curtis DJ, Rasmussen MA (2006) The evolution of cathemerality in primates and other mammals: a comparative and chronoecological approach. Folia Primatol 77:178-193
16. Curtis DJ, Zaramody A, Martin RD (1999) Cathemeral activity in the mongoose lemur, Eulemur mongoz. Am J Primatol 47:279-298
17. Curtis DJ, Donati G, Rasmussen MA (2006) Cathemerality. Folia Primatol 77:1-194
18. Daniels HL (1984) Oxygen consumption in Lemur fulvus: deviation from the ideal model. J Mammal 65:584-592
19. Demment M, van Soest PJ (1985) A nutritional explanation for body-size patterns of ruminant and non-ruminant herbivores. Am Nat 125:641-672
20. Dewar RE, Wallis JR (1999) Geographical patterning in intraannual rainfall variability in the tropics and near tropics: an L-moments approach. J Clim 12:3457-3466
21. Donati G (2002) Activity pattern of Eulemur fulvus collaris in relation to environmental variations in the littoral forest of Sainte Luce (Fort-Dauphin, Madagascar). PhD Thesis, University of Pisa
22. Donati G, Borgognini-Tarli SM (2006) Influence of abiotic factors on cathemeral activity: the case of Eulemur fulvus collaris in the littoral forest of Madagascar. Folia Primatol 77(1-2):104-122
23. Donati G, Lunardini A, Kappeler PM (1999) Cathemeral activity of red-fronted brown lemurs (Eulemur fulvus rufus) in the Kirindy Forest/CFPF. In: Rakotosamimanana B, Rasamimanana H, Ganzhorn JU, Goodman SM (eds) New directions in lemur studies. Plenum, New York, pp 119-137
24. Donati G, Lunardini A, Kappeler PM, Borgognini-Tarli SM (2001) Nocturnal activity in the cathemeral red-fronted lemur (Eulemur fulvus rufus), with observations during a lunar eclipse. Am J Primatol 53:69-78
25. Drack S, Ortmann S, Bührmann N, Schmid J, Warren RD, Heldmaier G, Ganzhorn JU (1999) Field metabolic rate and the cost of ranging of the red-tailed sportive lemur (Lepilemur ruficaudatus). In: Rakotosamimanana B, Rasamimanana H, Ganzhorn JU, Goodman SM (eds) New directions in lemur studies. Plenum, New York, pp 83-91
26. Dumetz N (1999) High plant diversity of lowland rainforest vestiges in eastern Madagascar. Biodivers Conserv 8:273-315
27. Dunbar RIM (1988) Primate social systems. Chapman & Hall, London
28. Dunbar RIM (1992) Time: a hidden constraint on the behavioural ecology of baboons. Behav Ecol Sociobiol 31:35-49
29. Engqvist A, Richard A (1991) Diet as a possible determinant of cathemeral activity patterns in primates. Folia Primatol 57:169-172
30. Erkert HG, Kappeler PM (2004) Arrived in the light: diel and seasonal activity patterns in wild Verreaux's sifakas (Propithecus v. verreauxi; Primates: Indridae). Behav Ecol Sociobiol 57:174-186
31. Fernandez-Duque E (2003) Influences of moonlight, ambient temperature, and food availability on the diurnal and nocturnal activity of owl monkeys (Aotus azarai). Behav Ecol Sociobiol 54:359-369
32. Ganzhorn JU, Wright PC, Ratsimbazafy J (1999) Primate communities: Madagascar. In: Fleagle JG, Janson C, Reed KE (eds) Primate communities. Cambridge University Press, Cambridge, pp 75-89
33. Ganzhorn JU, Klaus S, Ortmann S, Schmid J (2003) Adaptation to seasonality: some primate and non-primates examples. In: Kappeler PM, Pereira ME (eds) Primate life histories and socioecology. University of Chicago Press, Chicago, pp 132-148
34. Genoud M (2002) Comparative studies of basal rate of metabolism in primates. Evol Anthropol 11(Suppl):108-111
35. Goering HK, Soest PJ van (1970) Forage fiber analysis. USDA Handbook. N379, Washington DC
36. Goodman SM (2003) Predation on lemurs. In: Goodman SM, Benstead JP (eds) The natural history of Madagascar. University of Chicago Press, Chicago, pp 1221-1227
37. Grassi C (2001) The behavioural ecology of Hapalemur griseus griseus: the influence of microhabitat and population density on this small-bodied prosimian folivore. PhD Thesis, University of Austin
38. Halle S (2006) Polyphasic activity patterns in small mammals. Folia Primatol 77:15-26
39. Halle S, Stenseth NC (2000) Activity patterns in small mammals. An ecological approach. Springer, Berlin
40. Harvey PH, Pagel MD, Rees JA (1991) Mammalian metabolism and life histories. Am Nat 137:556-566
41. Heesy CP, Ross CF (2001) Evolution of activity patterns and chromatic vision in primates: morphometrics, genetics and cladistics. J Hum Evol 40:111-149
42. Hill WCO (1953) Primates, comparative anatomy and taxonomy. I. Strepsirhini. Edinburg Press, Edinburg
43. Hill RA, Barret L, Gaynor D, Weingrill T, Dixon P, Payne H, Henzi SP (2003) Day length, latitude and behavioural (in)flexibility in baboons (Papio cynocephalus ursinus). Behav Ecol Sociobiol 53:278-286
44. Jacobs GH (2002) Progress towards understanding the evolution of primate color vision. Evol Anthropol 11(Suppl 1):132-135
45. Janis C (1976) The evolutionary strategy of the Equidae and the origin of rumen and cecal digestion. Evolution 30:255-267
46. Jarman PJ (1974) The social organization of antelope in relation to their ecology. Behaviour 58:215-267
47. Jolly A (1966) Lemur behaviour. University of Chicago Press, Chicago
48. Johnson SE (2002) Ecology and speciation in brown lemurs: white-collared lemurs (Eulemur albocollaris) and hybrids (Eulemur albocollaris x Eulemur fulvus rufus) in southeastern Madagascar. PhD Thesis, University of Texas, Austin
49. Kappeler PM (1998) Nest, tree holes, and the evolution of primate life histories. Am J Primatol 46:7-33
50. Kappeler PM, Erkert HG (2003) On the move around the clock: correlates and determinants of cathemeral activity in wild redfronted lemurs (Eulemur fulvus rufus). Behav Ecol Sociobiol 54:359-369
51. Karpanty SM (2006) Direct and indirect impacts of raptors predation on lemurs of Southeastern Madagascar. Int J Primatol 27:239-261
52. Karpanty SM, Goodman SM (1999) Diet of the Madagascar Harrier-Hawk, Polyboroides radiatus, in Southeastern Madagascar. J Raptor Res 33:313-316
53. Kay R, Kirk EC (2000) Osteological evidence for the evolution of activity pattern and visual acuity in primates. Am J Phys Anthropol 113:235-262
54. Keys JE, van Soest PJ (1970) Digestibility of forages by the meadow vole (Microtus pennsylvanicus). J Dairy Sci 53:1502
55. Kirk EC (2006) Eye morphology in cathemeral lemurids and other mammals. Folia Primatol 77(1-2):27-49
56. Kleiber M (1961) The fire of life. Wiley, New York
57. Kurland JA, Gaulin SJC (1987) Comparability among measures of primate diets. Primates 28:71-77
58. Lambert JE (2002) Digestive retention times in forest guenons (Cercopithecus spp.) with reference to chimpanzees (Pan troglodytes). Int J Primatol 23:1169-1185
59. Martin RD (1990) Primate origins and evolution. Chapman & Hall, London
60. McNab BK (1978) Energetic of arboreal folivores: physiological problems and ecological consequences of feeding on an ubiquitous food supply. In: Montgomery GG (ed) The ecology of arboreal folivores. Smithsonian Institution Press, Washington DC, pp 153-162
61. McNab BK (1986) The influence of food habits on the energetic of eutherian mammals. Ecol Monogr 56:1-19
62. Milton K (1978) Behavioral adaptations to leaf-eating by the mantled howler monkey (Alouatta palliata). In: Montgomery GG (ed) The ecology of arboreal folivores. Smithsonian Press, Washington, DC, pp 535-550
63. Milton K (1981) Food choice and digestive strategies of two sympatric primate species. Am Nat 117:476-495
64. Milton K (1984) The role of food processing factors in primate food choice. In: Rodman PS, Cant JGH (eds) Adaptations for foraging in nonhuman primates: contribution to an organismal biology of prosimians, monkeys and apes. Columbia University Press, New York, pp 249-279
65. Milton K (1998) Physiological ecology of howlers (Alouatta): energetic and digestive considerations and comparison with colobinae. Int J Primatol 19:513-548
66. Morellato LPC, Talora DC, Takahasi A, Bencke CC, Romera EC, Zipparro VB (2000) Phenology of Atlantic rainforest trees: a comparative study. Biotropica 32:811-823
67. Morland HS (1993) Seasonal behavioral variation and its relationship to thermoregulation in ruffed lemurs (Varecia variegata variegata). In: Kappeler PM, Ganzhorn JU (eds) Lemur social systems and their ecological basis. Plenum, New York, pp 193-203
68. Müller EF (1985) Basal metabolic rates in primates: the possible role of phylogenetic and ecological factors. Comp Biochem Physiol 81: 707-711
69. Mutschler T (1999) Folivory in a small-bodied lemur: the nutrition of the Alaotran gentle lemur (Hapalemur griseus alaotrensis). In: Rakotosamimanana B, Rasamimanana H, Ganzhorn JU, Goodman SM (eds) New directions in lemur studies. Kluwer, New York, pp 221-239
70. Nash LT (1998) Vertical clingers and sleepers: seasonal influence on the activities and substrate use of Lepilemur leucopus at Beza Mahafaly Special Reserve, Madagascar. Folia Primatol 69:204-217
71. Nowak RM (1991) Walker's mammals of the world. The Johns Hopkins University Press, Baltimore
72. Oates JF, Swain T, Zantovska J (1977) Secondary compounds and food selection by Colobus monkeys. Biochem Syst Ecol 5:317-321
73. Ortmann S, Bradley BJ, Stolter C, Ganzhorn JU (2006) Estimating the quality and composition of wild animal diets - a critical survey of methods. In: Hohmann G, Robbins MM, Boesch C (eds) Feeding ecology in apes and other primates. Ecological, physical and behavioural aspects. Cambridge University Press, Cambridge, pp 395-418
74. Ossi K, Kamilar JM (2006) Environmental and phylogenetic correlates of Eulemur behavior and ecology (Primates: Lemuridae). Behav Ecol Sociobiol 61:53-64
75. Overdorff DJ (1988) Preliminary report on the activity cycle and diet of the red-bellied lemurs (Eulemur rubriventer) in Madagascar. Am J Primatol 16:143-153
76. Overdorff DJ (1993). Similarities, differences and seasonal patterns in the diets of Eulemur rubriventer and Eulemur fulvus rufus in the Ranomafana National Park, Madagascar. Int J Primatol 14:721-753
77. Overdorff DJ, Rasmussen MA (1995) Determinants of nighttime activity in "diurnal" lemurid primates. In: Alterman LG, Doyle GA, Izard K (eds) Creatures of the dark: the nocturnal prosimians. Plenum, New York, pp 61-74
78. Overdorff DJ, Strait SG, Telo A (1997) Seasonal variations in activity and diet in small bodied folivorous primates, Hapalemur griseus, southeastern Madagascar. Am J Primatol 43:211-223
79. Parra R (1978) Comparison of foregut and hindgut fermentation in herbivores. In: Montgomery GG (ed) The ecology of arboreal folivores. Smithsonian Press, Washington DC, pp 205-229
80. Pereira ME (1993) Seasonal adjustment of growth rate and adult body weight in ringtailed lemurs. In: Kappeler PM, Ganzhorn JU (eds) Lemur social systems and their ecological basis. Plenum, New York, pp 205-221
81. Pereira ME, Strohecker RA, Cavigelli SA, Hughes CL, Pearson, DD (1999) Metabolic strategy and social behavior in Lemuridae. In: Rakotosamimanana B, Rasamimanana H, Ganzhorn JU, Goodman SM (eds) New directions in lemur studies. Kluwer, New York, pp 93-118
82. Pollock JI (1979) Spatial distribution and ranging behavior in lemurs. In: Doyle GA, Martin RD (eds) The study of prosimian behavior. Academic, New York, pp 359-409
83. Powzyk JA (1997) The socio-ecology of two sympatric Indriids: Propithecus diadema diadema and Indri indri, a comparison of feeding strategies and their possible repercussions on speciesspecific behaviors. PhD Thesis, Duke University, Durham North Carolina
84. Rasmussen MA (1999) Ecological influences on activity cycle in two cathemeral primates, Eulemur mongoz (mongoose lemur) and Eulemur fulvus fulvus (common brown lemur). PhD Thesis, Duke University, Durham, North Carolina
85. Rasmussen MA (2005) Seasonality and predation risk: varying activity periods in lemurs and other primates. In: Brockman DK, van Schaik CP (eds) Seasonality in primates: implications for human evolution. Cambridge University Press, Cambridge, pp 105-128
86. Richard A (1977) The feeding behavior of Propithecus verreauxi. In: Clutton-Brock TH (ed) Primate ecology: studies of feeding and ranging behaviors in lemurs, monkeys, and apes. Academic, London, pp 71-96
87. Ross C (1992) Basal metabolic rate, body weight and diet in primates: an evaluation of the evidence. Folia Primatol 58:7-23
88. Roos C, Schmitz J, Zischler H (2004) Primate jumping genes elucidate strepsirrhine phylogeny. Proc Natl Acad Sci USA 101:10650-10654
89. Sailer LD, Gaulin SJC, Boster JS, Kurland JA (1985) Measuring the relationship between dietary quality and body size in primates. Primates 26:14-27
90. Schmid J, Ganzhorn JU (1996) Resting metabolic rate of Lepilemur ruficaudatus. Am J Primatol 38:169-174
91. Simmen B, Hladik A, Ramasiarisoa P (2003) Food intake and dietary overlap in native Lemur catta and Propithecus verreauxi and introduced Eulemur fulvus at Berenty, Southern Madagascar. Int J Primatol 24(5):949-968
92. Struhsaker TT (1975) The red colobus monkey. University of Chicago Press, Chicago
93. Sussman RW, Tattersall I (1976) Cycles of activity, group composition and diet of Lemur mongoz mongoz Linnaeus 1766 in Madagascar. Folia Primatol 26:270-283
94. 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
95. Tan I, Li WH (1999) Vision-Trichromatic vision in prosimians. Nature 402:36
96. Tan I, Yoder AD, Yamashita N, Wen-hsiung L (2005) Evidence from opsin genes rejects nocturnality in ancestral primates. Proc Natl Acad Sci USA 102:14712-14716
97. Tarnaud L (2006) Cathemerality in the Mayotte brown lemur (Eulemur fulvus): seasonality and food quality. Folia Primatol 77(1-2):166-177
98. Tattersall I (1979) Patterns of activity in the Mayotte lemur, Lemur fulvus mayottensis. J Mammal 60:314-323
99. Tattersall I (1982) The primates of Madagascar. Columbia University Press, New York
100. Tattersall I (1987) Cathemeral activity in primates: a definition. Folia Primatol 49:200-202
101. Tattersall I, Sussman RW (1975) Observations on the ecology and behavior of the mongoose lemur, Lemur mongoz mongoz Linnaeus (primates, lemuriformes) at Ampijoroa, Madagascar. Anthropol Papers Am Mus Nat Hist 52:195-216
102. van Schaik CP, Griffiths M (1996) Activity periods of Indonesian rainforest mammals. Biotropica 28:105-112
103. van Schaik CP, Kappeler PM (1996) The social systems of gregarious lemurs: lack of convergence with anthropoids due to evolutionary disequilibrium? Ethology 102:915-941
104. van Schaik CP, Madden R, Ganzhorn J (2005) Seasonality and primate communities. In: Brockman DK, van Schaik CP (eds) Seasonality in primates: implications for human evolution. Cambridge University Press, Cambridge, pp 445-463
105. van Soest PJ (1994) Nutritional ecology of the ruminants. Cornell University Press, Ithaca, New York
106. Vasey N (2000) Niche separation in Varecia variegata rubra and Eulemur fulvus albifrons: I. Interspecific patterns. Am J Phys Anthropol 112:411-431
107. Wright PC (1999) Lemur traits and Madagascar ecology: coping with an island environment. Yearb Phys Anthropol 42:31-72
108. Wright PC, Razafindratsita VR, Pochron ST, Jernvall J (2005) The key to Madagascar frugivores. In: Dew L, Boubli JP (eds) Tropical fruits and frugivores: the search for strong interactors. Springer, The Netherlands, pp 121-138
109. Yamashita N, Stoner KE, Riba-Hernandez P, Dominy NJ, Lucas PW (2005) Light levels used during feeding by primates species with different color vision phenotypes. Behav Ecol Sociobiol 58:618-629
110. Zielinsky WJ (2000) Weasels and martens - carnivores in northern latitudes. In: Halle S, Stenseth NC (eds) Activity patterns in small mammals: an ecological approach. Springer, Berlin, pp 95-118
111. Zinner D (1999) Relationship between feeding time and food intake in hamadryas baboons (Papio hamadryas) and the value of feeding time as predictor of food intake. Zoo Biol 18:495-505