Advertisement

Predator avoidance and dietary fibre predict diurnality in the cathemeral folivore Hapalemur meridionalis

  • Timothy M. Eppley
  • Julia Watzek
  • Jörg U. Ganzhorn
  • Giuseppe Donati
Original Article

Abstract

Though numerous mammalian taxa exhibit cathemerality (i.e. activity distributed across the 24-h cycle), this includes very few primates, exceptions being species from Aotinae and Lemuridae. Four non-mutually exclusive hypotheses have been proposed to explain the ultimate determinants for cathemeral activity in lemurs: thermoregulatory benefits, anti-predator strategy, competition avoidance and metabolic dietary-related needs. However, these have only been explored in the frugivorous genus Eulemur, with some species increasing nocturnality as a possible response to avoid diurnal raptors and to increase their ability to digest fibre during resource-scarce periods. Since Eulemur lack specializations for digesting bulk food, this strategy would allow for processing fibres over the full 24-h. The folivorous lemurids, i.e. genus Hapalemur, provide a divergent model to explore these hypotheses due to gastrointestinal adaptations for digesting dietary fibre and small body size compared to Eulemur. We linked continuous activity data collected from archival tags with observational behaviour and feeding data from three groups of adult Hapalemur meridionalis from January to December 2013. We tested the effects of thermoregulation, predator avoidance and the weighted proportion of digestible dietary fibre on the daily diurnal/nocturnal activity ratio using a Linear Mixed-Model. Our best-fit model revealed that increased canopy exposure and dietary fibre predicted greater diurnality. Our findings partly contrast with previous predictions for frugivorous lemurids. We propose a divergent adaptive explanation for folivorous lemurids. We suggest that the need to avoid terrestrial predators, as well as longer digestive bouts during bulk food periods, may override cathemerality in favour of diurnality in these bamboo lemurs.

Significance statement

Southern bamboo lemurs are active throughout the 24-h day, with high proportions of dietary fibre increasing diurnality, in contrast to other cathemeral primates. They also increase diurnality on days when using areas with greater canopy exposure, potentially avoiding nocturnal predators in risky foraging areas. We suggest that folivorous lemurids may require long periods of inactivity to conserve energy and digest dietary fibre, thus limiting activity to periods of optimal foraging efficiency over the 24-h cycle.

Keywords

Predator avoidance strategy Diel activity Dietary fibre Lunarphilia Southern bamboo lemur Thermoregulation 

Notes

Acknowledgments

We thank the Direction du Système des Aires Protégées and the Ministère de l’Environnement et Forêts of Madagascar for permission to conduct research. We are grateful to Jacques Rakotondranary and Tolona Andrianasolo for obtaining our research permits and to Katie Hall and Natalie Breden for assistance in the field. We also thank the Environment Team at QMM Rio Tinto for their assistance and provision of logistical support on-site and acknowledge their helpful staff, especially Jean-Baptiste Ramanamanjato, Johny Rabenantoandro, Faly Randriatafika, Laza Andriamandimbiarisoa, David Rabehevitra, Claude Soanary and Robertin Ravelomanantsoa. Many thanks are due to Irene Tomaschewski for the plant biochemical analyses. We would like to thank Maria van Noordwijk and two anonymous reviewers for their suggestions to improve previous versions of this manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical statement

This work was supported by the American Society of Primatologists, Conservation International (Primate Action Fund), Idea Wild, Mohamed bin Zayed Species Conservation Fund (Project Number: 11253008), Primate Conservation Inc. and Primate Society of Great Britain/Knowsley Safari Park. This research was carried out under the Accord de Collaboration between the Department of Animal Biology of the University of Antananarivo and the Department of Animal Ecology and Conservation of the University of Hamburg and QIT Madagascar Minerals (QMM). Research protocols were approved and permits authorized by the Commission Tripartite of the Direction des Eaux et Forêts de Madagascar (Autorisation de recherché No. 240/12/MEF/SG/DGF/DCB.SAP/SCB du 17 September 2012), adhering to the legal requirements of Madagascar. All data were collected in accordance with the ASAB/ABS Guidelines for Use of Animals in Research.

References

  1. Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–266PubMedCrossRefGoogle Scholar
  2. Andrews JR, Birkinshaw CR (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 69:175–182CrossRefGoogle Scholar
  3. Andriatsimietry R, Goodman SM, Razafimahatratra E, Jeglinski JWE, Marquard M, Ganzhorn JU (2009) Seasonal variation in the diet of Galidictis grandidieri Wozencraft, 1986 (Carnivora: Eupleridae) in a sub-arid zone of extreme south-western Madagascar. J Zool 279:410–415CrossRefGoogle Scholar
  4. Ankel-Simons F, Rasmussen DT (2008) Diurnality, nocturnality, and the evolution of primate visual systems. Am J Phys Anthropol 51:100–117CrossRefGoogle Scholar
  5. Aschoff J, Daan S, Groos GA (1982) Vertebrate circadian systems. Springer, BerlinCrossRefGoogle Scholar
  6. Aschoff J (1988) Masking of circadian rhythms by zeitgebers as opposed to entrainment. In: Hekkens WTJM, Kerkhof GA, Rietveld WJ (eds) Trends in chronobiology: advances in the biosciences. Pergamon Press, Oxford, pp. 149–161Google Scholar
  7. Ashby KR (1972) Patterns of daily activity in mammals. Mammal Rev 1:171–185CrossRefGoogle Scholar
  8. Bates D, Maechler M, Bolker B (2012) lme 4: Linear mixed-effects models using S4 classes. R package version 0.999375-42, http://CRAN.R-project.org/package=lme4
  9. Beier P, McCullough DR (1990) Factors influencing white-tailed deer activity patterns and habitat use. Wildlife Monogr 109:3–51Google Scholar
  10. Berger A, Scheibe KM, Eichhorn K, Scheibe A, Streich J (1999) Diurnal and ultradian rhythms of behaviour in a mare group of Przewalski horse (Equus ferus przewalskii), measured through one year under semi-reserve conditions. Appl Anim Behav Sci 64:1–17CrossRefGoogle Scholar
  11. Blanco MB, Dausmann KH, Ranaivoarisoa JF, Yoder AD (2013) Underground hibernation in a primate. Sci Rep 3:1768PubMedPubMedCentralCrossRefGoogle Scholar
  12. Bollen A, Donati G (2005) Phenology of the littoral forest of Sainte Luce, south-east Madagascar. Biotropica 37:32–43CrossRefGoogle Scholar
  13. Brockman DK (2003) Polyboroides radiatus predation attempts on Propithecus verreauxi. Folia Primatol 74:71–74PubMedCrossRefGoogle Scholar
  14. Brooke AP (2001) Population status and behaviours of the Samoan flying fox (Pteropus samoensis) on Tutuila Island, American Samoa. J Zool 254:309–319CrossRefGoogle Scholar
  15. Cabre-Vert N, Feistner ATC (1995) Comparative gut passage time in captive lemurs. Dodo 31:76–81Google Scholar
  16. Campbell JL, Eisemann JH, Williams CV, Glenn KM (2000) Description of the gastrointestinal tract of five lemur species: Propithecus tattersalli, Propithecus verreauxi coquereli, Varecia variegata, Hapalemur griseus, and Lemur catta. Am J Primatol 52:133–142PubMedCrossRefGoogle Scholar
  17. 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 64:323–335PubMedCrossRefGoogle Scholar
  18. 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: a multidisciplinary approach. Plenum Press, New York, pp. 69–88CrossRefGoogle Scholar
  19. Charles-Dominique P, Cooper HM, Hladik A, Hladik CM, Pages E, Pariente GF, Petter Rousseaux A, Petter JJ, Schilling A (1980) Nocturnal Malagasy primates: ecology, physiology and behavior. Academic Press, New YorkGoogle Scholar
  20. Chiarello AG (1998) Activity budgets and ranging patterns of the Atlantic forest maned sloth Bradypus torquatus (Xenarthra: Bradypodidae). J Zool 246:1–10CrossRefGoogle Scholar
  21. Chiesa JJ, Aguzzi J, Garcıa JA, Sarda F, de la Iglesia H (2010) Light intensity determines temporal niche switching of behavioral activity in deep water Nephrops norvegicus (Crustacea: Decapoda). J Biol Rhythm 25:277–287CrossRefGoogle Scholar
  22. Clarke JL, Jones ME, Jarman PJ (1995) Diurnal and nocturnal grouping and foraging behaviours of free-ranging eastern grey kangaroos. Aust J Zool 43:519–529CrossRefGoogle Scholar
  23. Cohen J, Cohen P, West SG, Aiken LS (2003) Applied multiple regression/correlation analysis for the behavioral sciences, 3rd edn. Erlbaum, Mahwah, New JerseyGoogle Scholar
  24. Colquhoun IC (2006) Predation and cathemerality: comparing the impact of predators on the activity patterns of lemurids and ceboids. Folia Primatol 77:143–165PubMedCrossRefGoogle Scholar
  25. Colquhoun IC (2007) Anti-predator strategies of cathemeral primates: dealing with predators of the day and the night. In: Gursky S, Nekaris KAI (eds) Primate anti-predator strategies. Springer, New York, pp. 146–172CrossRefGoogle Scholar
  26. Cork SJ, Foley WJ (1991) Digestive and metabolic strategies of arboreal mammalian folivores in relation to chemical defences in temperate and tropical forests. In: Palo RT, Robbins CT (eds) Plant defences against mammalian herbivory. CRC Press, Boca Raton, FL, pp. 133–166Google Scholar
  27. Cowan CA, Peckarsky BL (1994) Diel feeding and positioning periodicity of a grazing mayfly in a trout stream and a fishless stream. Can J Fish Aquat Sci 51:450–459CrossRefGoogle Scholar
  28. Cowlishaw G (1997) Trade-offs between foraging and predation risk determine habitat use in a desert baboon population. Anim Behav 53:241–253CrossRefGoogle Scholar
  29. Curtis DJ, Zaramody A, Martin RD (1999) Cathemerality in the mongoose lemur, Eulemur mongoz. Am J Primatol 47:279–298PubMedCrossRefGoogle Scholar
  30. Curtis DJ, Rasmussen MA (2002) Cathemerality in lemurs. Evol Anthropol 11(Suppl):83–86Google Scholar
  31. Curtis DJ, Rasmussen MA (2006) The evolution of cathemerality in primates and other mammals: a comparative and chronoecological approach. Folia Primatol 77:178–193PubMedCrossRefGoogle Scholar
  32. Daan S, Slopsema S (1978) Short-term rhythms in foraging behaviour in the common vole, Microtus arvalis. J Comp Physiol A 127:215–227CrossRefGoogle Scholar
  33. Dausmann KH (2014) Flexible patterns in energy savings: heterothermy in primates. J Zool 292:101–111CrossRefGoogle Scholar
  34. Dewar RE, Richard AF (2007) Evolution in the hypervariable environment of Madagascar. P Natl Acad Sci USA 104:13723–13727CrossRefGoogle Scholar
  35. Donati G, Baldi N, Morelli V, Ganzhorn JU, Borgognini-Tarli SM (2009) Proximate and ultimate determinants of cathemeral activity in brown lemurs. Anim Behav 77:317–325CrossRefGoogle Scholar
  36. Donati G, Bollen A, Borgognini-Tarli S, Ganzhorn JU (2007a) Feeding over the 24-h cycle: dietary flexibility of cathemeral collared lemurs (Eulemur collaris). Behav Ecol Sociobiol 61:1237–1251CrossRefGoogle Scholar
  37. Donati G, Borgognini-Tarli SM (2006a) Influence of abiotic factors on cathemeral activity: the case of Eulemur fulvus collaris in the littoral forest of Madagascar. Folia Primatol 77:104–122PubMedCrossRefGoogle Scholar
  38. Donati G, Borgognini-Tarli SM (2006b) From darkness to daylight: cathemeral activity in primates. J Anthropol Sci 84:7–32Google Scholar
  39. Donati G, Campera M, Balestri M, Serra V, Barresi M, Schwitzer C, Curtis DJ, Santini L (2016) Ecological and anthropogenic correlates of activity patterns in Eulemur. Int J Primatol 37:29–46CrossRefGoogle Scholar
  40. 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 Press, New York, pp. 119–137CrossRefGoogle Scholar
  41. 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 53:69–78PubMedCrossRefGoogle Scholar
  42. Donati G, Ramanamanjato JB, Ravoahangy AM, Vincelette M (2007b) Translocation as a conservation measure for a threatened species: the case of Eulemur collaris in the Mandena littoral forest, south-eastern Madagascar. In: Ganzhorn JU, Goodman SM, Vincelette M (eds) Biodiversity, ecology, and conservation of the littoral ecosystems in southeastern Madagascar, Tolagnaro (Fort Dauphin). Smithsonian Institution Press, Washington, DC, pp. 237–243Google Scholar
  43. Donati G, Santini L, Razafindramanana J, Boitani L, Borgognini-Tarli S (2013) Unexpected nocturnal activity in “diurnal” Lemur catta supports cathemerality as one of the key adaptations of the lemurid radiation. Am J Phys Anthropol 150:99–106PubMedCrossRefGoogle Scholar
  44. Engqvist A, Richard A (1991) Diet as a possible determinant of cathemeral activity patterns in primates. Folia Primatol 57:169–172PubMedCrossRefGoogle Scholar
  45. Enright JT (1970) Ecological aspects of endogenous rhythmicity. Annu Rev Ecol Syst 1:221–238CrossRefGoogle Scholar
  46. Eppley TM, Donati G, Ganzhorn JU (2016a) Determinants of terrestrial feeding in an arboreal primate: the case of the southern bamboo lemur (Hapalemur meridionalis). Am J Phys Anthropol 161:328–342PubMedCrossRefGoogle Scholar
  47. Eppley TM, Donati G, Ganzhorn JU (2016b) Unusual sleeping site selection by southern bamboo lemurs. Primates 57:167–173PubMedCrossRefGoogle Scholar
  48. Eppley TM, Donati G, Ramanamanjato J-B, Randriatafika F, Andriamandimbiarisoa LN, Rabehevitra D, Ravelomanantsoa R, Ganzhorn JU (2015b) The use of an invasive species habitat by a small folivorous primate: implications for conservation. PLoS One 10:e0140981PubMedPubMedCentralCrossRefGoogle Scholar
  49. Eppley TM, Ganzhorn JU, Donati G (2015a) Cathemerality in a small, folivorous primate: proximate control of diel activity in Hapalemur meridionalis. Behav Ecol Sociobiol 69:991–1002CrossRefGoogle Scholar
  50. Eppley TM, Ganzhorn JU, Donati G (2016c) Latrine behaviour as a multimodal communicatory signal station in wild lemurs: the case of Hapalemur meridionalis. Anim Behav 111:57–67CrossRefGoogle Scholar
  51. Eppley TM, Hall K, Donati G, Ganzhorn JU (2015c) An unusual case of affiliative association of a female Lemur catta in a Hapalemur meridionalis social group. Behaviour 152:1041–1061CrossRefGoogle Scholar
  52. Eppley TM, Ravelomanantsoa R (2015) Predation of an adult southern bamboo lemur Hapalemur meridionalis by a Dumeril’s boa Acrantophis dumerili. Lemur News 19:2–3Google Scholar
  53. 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 52:7–13PubMedCrossRefGoogle Scholar
  54. Erkert HG (1989) Lighting requirements of nocturnal primates in captivity: a chronobiological approach. Zoo Biol 8:179–191CrossRefGoogle Scholar
  55. Erkert HG (2011) Chronobiological aspects of primate research. In: Setchell JM, Curtis DJ (eds) Field and laboratory methods in primatology: a practical guide. Cambridge University Press, Cambridge, pp. 319–338CrossRefGoogle Scholar
  56. Erkert HG, Cramer B (2006) Chronobiological background to cathemerality: circadian rhythms in Eulemur fulvus albifrons (Prosimii) and Aotus azarai boliviensis (Anthropoidea). Folia Primatol 77:87–103PubMedCrossRefGoogle Scholar
  57. Fausser JL, Prosper P, Donati G, Ramanamanjato J-B, Rumpler Y (2002) Phylogenetic relationships between Hapalemur species and subspecies based on mitochondrial DNA sequences. BMC Evol Biol 2:4PubMedPubMedCentralCrossRefGoogle Scholar
  58. Fernández-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 54:359–369CrossRefGoogle Scholar
  59. Fernández-Duque E, de la Iglesia H, Erkert HG (2010) Moonstruck primates: owl monkeys (Aotus) need moonlight for nocturnal activity in their natural environment. PLoS One 5:e12572PubMedPubMedCentralCrossRefGoogle Scholar
  60. Fernández-Duque E, Erkert HG (2006) Cathemerality and lunar periodicity of activity rhythms in owl monkeys of the Argentinian Chaco. Folia Primatol 77:123–138PubMedCrossRefGoogle Scholar
  61. Fidgett AL, Feistner ATC, Galbraith H (1996) Dietary intake, food composition and nutrient intake in captive Alaotran gentle lemurs Hapalemur griseus alaotrensis. Dodo 32:44–62Google Scholar
  62. Field A (2013) Discovering statistics using SPSS, 4th edn. Sage, LondonGoogle Scholar
  63. Flowerdew JR (2000) Wood mice—small granivores/insectivores with seasonally variable patterns. In: Halle S, Stenseth NC (eds) Activity patterns in small mammals: an ecological approach. Springer, Berlin, pp. 177–189CrossRefGoogle Scholar
  64. Ganzhorn JU (1989) Niche separation of seven lemur species in the eastern rainforest of Madagascar. Oecologia 79:279–286PubMedCrossRefGoogle Scholar
  65. Gilmore DP, Da Costa CP, Duarte DPF (2001) Sloth biology: an update on their physiological ecology, behavior and role as vectors of arthropods and arboviruses. Braz J Med Biol Res 34:9–25PubMedCrossRefGoogle Scholar
  66. Grassi C (2002) Sex differences in feeding, height, and space use in Hapalemur griseus. Int J Primatol 23:677–693CrossRefGoogle Scholar
  67. Grassi C (2006) Variability in habitat, diet, and social structure of Hapalemur griseus in Ranomafana National Park, Madagascar. Am J Phys Anthropol 131:50–63PubMedCrossRefGoogle Scholar
  68. Greenwood MFD, Metcalfe NB (1998) Minnows become nocturnal at low temperatures. J. Fish Biol 53:25–32CrossRefGoogle Scholar
  69. Gunn J, Hawkins D, Barnes RF, Mofulu F, Grant RA, Norton GW (2014) The influence of lunar cycles on crop-raiding elephants; evidence for risk avoidance. Afr J Ecol 52:129–137CrossRefGoogle Scholar
  70. Gursky S (2003) Lunar philia in a nocturnal prosimian primate. Int J Primatol 24:351–367CrossRefGoogle Scholar
  71. Halle S (1995) Diel pattern of locomotor activity in populations of root voles, Microtus oeconomus. J Biol Rhythm 10:211–224CrossRefGoogle Scholar
  72. Halle S (2000) Voles—small graminivores with polyphasic patterns. In: Halle S, Stenseth NC (eds) Activity patterns in small mammals: an ecological approach. Springer, Berlin, pp. 191–215CrossRefGoogle Scholar
  73. Halle S (2006) Polyphasic activity patterns in small mammals. Folia Primatol 77:15–26PubMedCrossRefGoogle Scholar
  74. Halle S, Stenseth NC (2000) Activity patterns in small mammals: an ecological approach. Springer, BerlinCrossRefGoogle Scholar
  75. Holley AJF (2001) The daily activity period of the brown hare (Lepus europaeus). Mammal Biol 66:357–364Google Scholar
  76. Horning M, Trillmich F (1999) Lunar cycles in diel prey migrations exert a stronger effect on the diving of juveniles than adult Galapagos fur seals. Proc R Soc Lond B 266:1127–1132CrossRefGoogle Scholar
  77. Jacob J, Brown JS (2000) Microhabitat use, giving-up densities and temporal activity as short and long-term anti-predator behaviors in common voles. Oikos 91:131–138CrossRefGoogle Scholar
  78. Janson CH (1998) Testing the predation hypothesis for vertebrate sociality: prospects and pitfalls. Behaviour 135:389–410CrossRefGoogle Scholar
  79. Jones M, Mandelik Y, Dayan T (2001) Coexistence of temporally partitioned spiny mice: roles of habitat structure and foraging behavior. Ecology 82:2164–2176CrossRefGoogle Scholar
  80. Kaczensky P, Huber D, Knauer F, Roth H, Wagner A, Kusak J (2006) Activity patterns of brown bears (Ursus arctos) in Slovenia and Croatia. J Zool 269:474–485CrossRefGoogle Scholar
  81. 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 54:359–369CrossRefGoogle Scholar
  82. Karpanty SM (2006) Direct and indirect impacts of raptor predation on lemurs in southeastern Madagascar. Int J Primatol 27:239–261CrossRefGoogle Scholar
  83. Karpanty SM, Wright PC (2007) Predation on lemurs in the rainforest of Madagascar by multiple predator species: observations and experiments. In: Gursky S, Nekaris KAI (eds) Primate anti-predator strategies. Springer, New York, pp. 77–99CrossRefGoogle Scholar
  84. Kirk EC (2006) Eye morphology in cathemeral lemurids and other mammals. Folia Primatol 77:27–49PubMedCrossRefGoogle Scholar
  85. Kronfeld-Schor N, Dayan T (1999) The dietary basis for temporal partitioning: food habits of coexisting Acomys species. Oecologia 121:123–128PubMedCrossRefGoogle Scholar
  86. Kurland JA, Gaulin SJC (1987) Comparability among measures of primate diets. Primates 28:71–77CrossRefGoogle Scholar
  87. Lambert JE (2002) Digestive retention times in forest guenons (Cercopithecus spp.) with reference to chimpanzees (Pan troglodytes). Int J Primatol 23:1169–1185CrossRefGoogle Scholar
  88. Lang AB, Kalko EKV, Romer H, Bockholdt C, Dechmann DKN (2006) Activity levels of bats and katydids in relation to the lunar cycle. Oecologia 146:659–666PubMedCrossRefGoogle Scholar
  89. Lode T (1995) Activity pattern of polecats Mustela putorius L. in relation to food habits and prey activity. Ethology 100:295–308CrossRefGoogle Scholar
  90. Marcelli M, Fusillo R, Boitani L (2003) Sexual segregation in the activity patterns of European polecats (Mustela putorius). J Zool 261:249–255CrossRefGoogle Scholar
  91. Martin RD (1972) Adaptive radiation and behaviour of the Malagasy lemurs. Philos T Roy Soc B 264:320–352CrossRefGoogle Scholar
  92. Martin RD (1990) Primate origins and evolution: a phylogenetic reconstruction. Chapman & Hall, LondonGoogle Scholar
  93. McComb K, Shannon G, Sayialel KN, Moss C (2014) Elephants can determine ethnicity, gender, and age from acoustic cues in human voices. P Natl Acad Sci USA 111:5433–5438CrossRefGoogle Scholar
  94. Merritt JF, Vessey SH (2000) Shrews—small insectivores with polyphasic patterns. In: Halle S, Stenseth NC (eds) Activity patterns in small mammals: an ecological approach. Springer, Berlin, pp. 235–251CrossRefGoogle Scholar
  95. Metcalfe N, Fraser N, Burns M (1999) Food availability and the nocturnal vs. diurnal foraging trade-off in juvenile salmon. J Anim Ecol 68:371–381CrossRefGoogle Scholar
  96. Miller LE (2002) An introduction to predator sensitive foraging. In: Miller LE (ed) Eat or be eaten: predator sensitive foraging among primates. Cambridge University Press, Cambridge, pp. 1–17CrossRefGoogle Scholar
  97. Milton K (1981) Food choice and digestive strategies of two sympatric primate species. Am Nat 117:476–495CrossRefGoogle Scholar
  98. Milton K (1998) Physiological ecology of howlers (Alouatta): energetic and digestive considerations and comparison with the Colobinae. Int J Primatol 19:513–548CrossRefGoogle Scholar
  99. Mrosovsky N (1999) Masking: history, definitions, and measurement. Chronobiol Int 16:415–429PubMedCrossRefGoogle Scholar
  100. 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. Plenum Press, New York, pp. 221–239CrossRefGoogle Scholar
  101. Nash LT (2007) Moonlight and behavior in nocturnal and cathemeral primates, especially Lepilemur leucopus: illuminating possible anti-predator efforts. In: Gursky S, Nekaris KAI (eds) Primate anti-predator strategies. Springer, New York, pp. 173–205CrossRefGoogle Scholar
  102. Orpwood JE, Griffiths SW, Armstrong JD (2006) Effects of food availability on temporal activity patterns and growth of Atlantic salmon. J Anim Ecol 75:677–685PubMedCrossRefGoogle Scholar
  103. Orrock JL, Danielson BJ, Brinkerhoff R (2004) Rodent foraging is affected by indirect, but not by direct, cues of predation risk. Behav Ecol 15:433–437CrossRefGoogle Scholar
  104. 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. Cambridge University Press, Cambridge, pp. 395–418Google Scholar
  105. Overdorff DJ (1988) Preliminary report on the activity cycle and diet on the red-bellied lemurs (Eulemur rubriventer) in Madagascar. Am J Primatol 16:143–153CrossRefGoogle Scholar
  106. Overdorff DJ, Rasmussen MA (1995) Determinants of nighttime activity in ‘diurnal’ lemurid primates. In: Alterman LG, Doyle GA, Izard MK (eds) Creatures of the dark: the nocturnal prosimians. Plenum Press, New York, pp. 61–74CrossRefGoogle Scholar
  107. 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 43:211–223PubMedCrossRefGoogle Scholar
  108. Packer C, Swanson A, Ikanda D, Kushnir H (2011) Fear of darkness, the full moon and the nocturnal ecology of African lions. PLoS One 6:e22285PubMedPubMedCentralCrossRefGoogle Scholar
  109. Palomares F, Delibes M (2000) Mongooses, civets and genets—carnivores in southern latitudes. In: Halle S, Stenseth NC (eds) Activity patterns in small mammals: an ecological approach. Springer, Berlin, pp. 119–130CrossRefGoogle Scholar
  110. Penteriani V, Kuparinen A, Delgado MM, Lourenço R, Campioni L (2011) Individual status, foraging effort and need for conspicuousness shape behavioural responses of a predator to moon phases. Anim Behav 82:413–420CrossRefGoogle Scholar
  111. Perrin MR (2013) The gastrointestinal anatomy of the lesser bamboo lemur, Hapalemur griseus, with comments on digestive function. S Afr J Wildl Res 43:79–83CrossRefGoogle Scholar
  112. Polat ES, Coskun B, Gurbuz E, Balevi T (2013) The effects of roughage type on the daily patterns of feed intake and eating behaviour in young sheep. Rev Med Vet-Toulouse 164:503–510Google Scholar
  113. Prugh LR, Golden CD (2014) Does moonlight increase predation risk? Meta-analysis reveals divergent responses of nocturnal mammals to lunar cycles. J Anim Ecol 83:504–514PubMedCrossRefGoogle Scholar
  114. Rasmussen MA (1999) Ecological influences on activity cycle in two cathemeral primates, Eulemur mongoz (mongoose lemur) and Eulemur fulvus fulvus (common brown lemur). PhD Dissertation, Duke UniversityGoogle Scholar
  115. Rasmussen MA (2005) Seasonality in predation risk: varying activity periods in lemurs and other primates. In: Brockman DK, van Schaik CP (eds) Primate seasonality: implications for human evolution. Cambridge University Press, Cambridge, pp. 105–128CrossRefGoogle Scholar
  116. R Development Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, http://www.R-project.org/
  117. Reebs SG (2002) Plasticity of diel and circadian activity rhythms in fishes. Rev Fish Biol Fisher 12:349–371CrossRefGoogle Scholar
  118. Rezende EL, Cortes A, Bacigalupe LD, Nespolo RF, Bozinovic F (2003) Ambient temperature limits above-ground activity of the subterranean rodent Spalacopus cyanus. J Arid Environ 55:63–74CrossRefGoogle Scholar
  119. Rothman JM, Chapman CA, van Soest PJ (2012) Methods in primate nutritional ecology: a user’s guide. Int J Primatol 33:542–566CrossRefGoogle Scholar
  120. Rydell J, Speakman J (1995) Evolution of nocturnality in bats: potential competitors and predators during their early history. Biol J Linn Soc 54:183–191CrossRefGoogle Scholar
  121. Santini L, Rojas D, Donati G (2015) Evolving through day and night: origin and diversification of activity pattern in modern primates. Behav Ecol 26:789–796CrossRefGoogle Scholar
  122. Schlichting M, Grebler R, Menegazzi P, Helfrich-Förster C (2015) Twilight dominates over moonlight in adjusting drosophila’s activity pattern. J Biol Rhythm 30:117–128CrossRefGoogle Scholar
  123. Schoener TW (1971) Theory of feeding strategies. Annu Rev Ecol Syst 2:369–404CrossRefGoogle Scholar
  124. Schwitzer N, Kaumanns W, Seitz PC, Schwitzer C (2007) Cathemeral activity patterns of the blue-eyed black lemur Eulemur macaco flavifrons in intact and degraded forest fragments. Endanger Species Res 3:239–247Google Scholar
  125. Serena M (1994) Use of time and space by platypus (Ornithorhynchus anatinus: Monotremata) along a Victorian stream. J Zool 232:117–131CrossRefGoogle Scholar
  126. Singmann H (2014) afex: analysis of factorial experiments. R package (version 0.9-109), http://CRAN.R-project.org/package=afex
  127. 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 20:547–566CrossRefGoogle Scholar
  128. Tarnaud L (2006) Cathemerality in the Mayotte brown lemur (Eulemur fulvus): seasonality and food quality. Folia Primatol 77:166–177PubMedCrossRefGoogle Scholar
  129. Tattersall I (1979) Patterns of activity in the Mayotte brown lemur, Lemur fulvus mayottensis. J Mammal 60:314–323CrossRefGoogle Scholar
  130. Tattersall I (1987) Cathemeral activity in primates: a definition. Folia Primatol 49:200–202CrossRefGoogle Scholar
  131. Tattersall I (2008) Avoiding commitment: cathemerality among primates. Biol Rhythm Res 39:213–228CrossRefGoogle Scholar
  132. Taylor WA, Skinner JD (2003) Activity patterns, home ranges and burrow use of aardvarks (Orycteropus afer) in the Karoo. J Zool 261:291–297CrossRefGoogle Scholar
  133. van Schaik CP (1983) Why are diurnal primates living in groups? Behaviour 87:120–144CrossRefGoogle Scholar
  134. van Schaik CP, Griffiths M (1996) Activity periods of Indonesian rain forest mammals. Biotropica 28:105–112CrossRefGoogle Scholar
  135. van Schaik CP, Kappeler PM (1993) Life history, activity period and lemur social systems. In: Kappeler PM, Ganzhorn JU (eds) Lemur social systems and their ecological basis. Plenum Press, New York, pp. 241–260CrossRefGoogle Scholar
  136. van Schaik CP, Kappeler PM (1996) The social system of gregarious lemurs: lack of convergence with anthropoids due to evolutionary disequilibrium? Ethology 102:915–941CrossRefGoogle Scholar
  137. van Schaik CP, van Noordwijk MA (1989) The special role of male Cebus monkeys in predation avoidance and its effect on group composition. Behav Ecol Sociobiol 24:265–276CrossRefGoogle Scholar
  138. van Soest PJ (1996) Allometry and ecology of feeding behavior and digestive capacity in herbivores: a review. Zoo Biol 15:455–479CrossRefGoogle Scholar
  139. Wallis IR, Edwards MJ, Windley H, Krockenberger AK, Felton A, Quenzer M, Ganzhorn JU, Foley WJ (2012) Food for folivores: nutritional explanations linking diets to population density. Oecologia 169:281–291PubMedCrossRefGoogle Scholar
  140. Wauters LA (2000) Medium-sized granivores in woodland habitats. In: Halle S, Stensteth NC (eds) Activity patterns in small mammals: an ecological approach. Springer, Berlin, pp. 131–144CrossRefGoogle Scholar
  141. Wolfe JL, Summerlin CT (1989) The influence of lunar light on nocturnal activity of the old field mouse. Anim Behav 37:410–414CrossRefGoogle Scholar
  142. Wright PC (1989) The nocturnal primate niche in the New World. J Hum Evol 18:635–658CrossRefGoogle Scholar
  143. Wright PC (1998) Impact of predation risk on the behaviour of Propithecus diadema edwardsi in the rain forest of Madagascar. Behaviour 135:483–512CrossRefGoogle Scholar
  144. Wright PC (1999) Lemur traits and Madagascar ecology: coping with an island environment. Yrbk Phys Anthropol 42:31–72CrossRefGoogle Scholar
  145. Zalewski A (2000) Factors affecting the duration of activity by pine martens (Martes martes) in the Białowieża National Park, Poland. J Zool 251:439–447Google Scholar
  146. Zielinsky WJ (1988) The influence of daily variation in foraging cost on the activity of small carnivores. Anim Behav 36:239–249CrossRefGoogle Scholar
  147. 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. 95–118CrossRefGoogle Scholar
  148. Zschille J, Stier N, Roth M (2010) Gender differences in activity patterns of American mink Neovison vison in Germany. Eur J Wildlife Res 56:187–194CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Timothy M. Eppley
    • 1
    • 2
    • 3
  • Julia Watzek
    • 4
  • Jörg U. Ganzhorn
    • 2
  • Giuseppe Donati
    • 3
  1. 1.Department of AnthropologyUniversity of TexasAustinUSA
  2. 2.Biozentrum Grindel, Department of Animal Ecology and ConservationUniversity of HamburgHamburgGermany
  3. 3.Nocturnal Primate Research Group, Department of Social SciencesOxford Brookes UniversityOxfordUK
  4. 4.Language Research Center, Department of PsychologyGeorgia State UniversityAtlantaUSA

Personalised recommendations