Skip to main content
SpringerLink
Log in

Cathemerality in a small, folivorous primate: proximate control of diel activity in Hapalemur meridionalis

  • Original Paper
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

Abstract

A non-adherence to a strict diurnal or nocturnal activity cycle is prevalent among mammals, including taxa of Lemuridae, but rare among other primates. While non-mutually exclusive ecological hypotheses attempted to explain the evolution of this activity, termed cathemerality, as either an old or a recent phenomenon, the scarcity of systematic data collected over 24 h limits our potential to explore its proximate and ultimate determinants. Among strepsirrhines, systematic studies involving only two lemurid genera (Eulemur and Lemur) have recorded this activity pattern, while fewer quantitative observations are available for other taxa. If cathemerality could be shown in most members of Lemuridae despite their different ecological adaptations, this would support the hypothesis that this trait is basal and appeared early during lemurid evolution. Here, we investigated whether the folivorous southern bamboo lemur (Hapalemur meridionalis) exhibits cathemeral activity, and determined which environmental factors influence its pattern. We deployed ten archival tags across four social groups to continuously record activity data over a 15-month period. This allowed us to generate a diurnal/nocturnal (DN) ratio for each 24-h period and assess their diel activity. Our data suggest that southern bamboo lemurs are cathemeral within Mandena; while climatic factors showed no influence, nocturnal activity increased with greater nocturnal luminance. Despite contrasting dietary niches, visual morphologies, and body sizes between Hapalemur, Eulemur, and Lemur, all three exhibit cathemerality and lunarphilia. The close phylogenetic proximity of these lemurids supports this flexible activity pattern as an ancestral trait that likely dates to the origin of the Lemuridae radiation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Agetsuma N, Nakagawa N (1998) Effects of habitat differences on feeding behaviors of Japanese monkeys: comparison between Yakushima and Kinkazan. Primates 39:275–289

    Google Scholar 

  • 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

    Google Scholar 

  • Ankel-Simons F, Rasmussen DT (2008) Diurnality, nocturnality, and the evolution of primate visual systems. Am J Phys Anthropol 51:100–117

    Google Scholar 

  • Aschoff J, Daan S, Honma KI (1982) Zeitgebers, entrainment, and masking: some unsettled questions. In: Aschoff J, Daan S, Groos GA (eds) Vertebrate circadian systems. Springer, Berlin, pp 13–24

    Google Scholar 

  • Ashby KR (1972) Patterns of daily activity in mammals. Mammal Rev 1:171–185

    Google Scholar 

  • Bearder SK, Nekaris KAI, Buzzell CA (2001) Dangers in the night: are some nocturnal primates afraid of the dark? In: Miller LE (ed) Eat or be eaten: predator sensitive foraging among primates. Cambridge University Press, Cambridge, pp 21–43

    Google Scholar 

  • Bearder SK, Nekaris KAI, Curtis DJ (2006) A re-evaluation of the role of vision in the activity and communication of nocturnal primates. Folia Primatol 77:50–71

    CAS  PubMed  Google Scholar 

  • Bollen A, Donati G (2005) Phenology of the littoral forest of Sainte Luce, south-east Madagascar. Biotropica 37:32–43

    Google Scholar 

  • 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: an interdisciplinary approach. Plenum Press, New York, pp 69–88

    Google Scholar 

  • 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, New York

    Google Scholar 

  • 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 25:277–287

    Google Scholar 

  • Colquhoun IC (1998) Cathemeral behaviour of Eulemur macaco macaco at Ambato Massif, Madagascar. Folia Primatol 69:22–34

    Google Scholar 

  • Corsini MT, Lovari S, Sonnino S (1995) Temporal activity patterns of crested porcupines Hystrix cristata. J Zool 236:43–54

    Google Scholar 

  • Cresswell WJ, Harris S (1988) The effects of weather conditions on the movements and activity of badgers (Meles meles) in a suburban environment. J Zool 216:187–194

    Google Scholar 

  • Curtis DJ, Rasmussen MA (2002) Cathemerality in lemurs. Evol Anthropol 11:83–86

    Google Scholar 

  • Curtis DJ, Rasmussen MA (2006) The evolution of cathemerality in primates and other mammals: a comparative and chronoecological approach. Folia Primatol 77:178–193

    CAS  PubMed  Google Scholar 

  • Curtis DJ, Zaramody A, Martin RD (1999) Cathemerality in the mongoose lemur, Eulemur mongoz. Am J Primatol 47:279–298

    CAS  PubMed  Google Scholar 

  • Daan S, Slopsema S (1978) Short-term rhythms in foraging behaviour in the common vole, Microtus arvalis. J Comp Physiol A 127:215–227

    Google Scholar 

  • Dewar RE (1997) Were people responsible for the extinction of Madagascar’s subfossils, and how will we ever know? In: Goodman SM, Patterson BD (eds) Natural change and human impact in Madagascar. Smithsonian Institution Press, Washington, pp 364–377

    Google Scholar 

  • Dewar RE, Radimilahy C, Wright HT, Jacobs Z, Kelly GO, Berna F (2013) Stone tools and foraging in northern Madagascar challenge Holocene extinction models. Proc Natl Acad Sci U S A 110:12583–12588

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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 77:104–122

    PubMed  Google Scholar 

  • 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 119–137

    Google Scholar 

  • Donati G, Lunardini A, Kappeler PM, Borgognini-Tarli SM (2001) Nocturnal activity in the cathemeral redfronted lemur (Eulemur fulvus rufus), with observations during a lunar eclipse. Am J Primatol 53:69–78

    CAS  PubMed  Google Scholar 

  • 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 61:1237–1251

    Google Scholar 

  • 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 of south-eastern Madagascar. Smithsonian Institution Press, Washington, pp 237–243

    Google Scholar 

  • Donati G, Baldi N, Morelli V, Ganzhorn JU, Borgognini-Tarli SM (2009) Proximate and ultimate determinants of cathemeral activity in brown lemurs. Anim Behav 77:317–325

    Google Scholar 

  • Donati G, Santini L, Razafindramanana J, Boitani L, Borgognini‐Tarli S (2013) (Un‐)expected nocturnal activity in “diurnal” Lemur catta supports cathemerality as one of the key adaptations of the lemurid radiation. Am J Phys Anthropol 150:99–106

    PubMed  Google Scholar 

  • Dumetz N (1999) High plant diversity of lowland rainforest vestiges in eastern Madagascar. Biodivers Conserv 8:273–315

    Google Scholar 

  • Dyer MA, Martins R, da Silva Filho M, Muniz JAP, Silveira LCL, Cepko CL, Finlay BL (2009) Developmental sources of conservation and variation in the evolution of the primate eye. Proc Natl Acad Sci U S A 106:8963–8968

    PubMed Central  CAS  PubMed  Google Scholar 

  • Engqvist A, Richard A (1991) Diet as a possible determinant of cathemeral activity patterns in primates. Folia Primatol 57:169–172

    CAS  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Eppley TM, Hall K, Donati G, Ganzhorn JU (2015) An unusual case of affiliative association of a female Lemur catta in a Hapalemur meridionalis social group. Behaviour (published online, doi:10.1163/1568539X-00003267)

  • Erkert HG (1974) Der einfl uss des mondlichtes auf die aktivitätsperiodik nachtaktiver säugetiere. Oecologia 14:269–287

    Google Scholar 

  • Erkert HG (1976) Lunar periodic variation of the phase angle difference in nocturnal animals under natural zeitgeber conditions near the equator. Int J Chronobiol 4:125–138

    CAS  PubMed  Google Scholar 

  • Erkert HG (1989) Lighting requirements of nocturnal primates in captivity: a chronobiological approach. Zoo Biol 8:179–191

    Google Scholar 

  • Erkert HG (2003) Chronobiological aspects of primate research. In: Setchell JM, Curtis DJ (eds) Field and laboratory methods in primatology. Cambridge University Press, Cambridge, pp 252–270

    Google Scholar 

  • Erkert HG, Kappeler PM (2004) Arrived in the light: diel and seasonal activity patterns in wild Verreaux’s sifakas (Propithecus v. verreauxi; Primates: Indriidae). Behav Ecol Sociobiol 57:174–186

    Google Scholar 

  • 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 2:4

    PubMed Central  PubMed  Google Scholar 

  • 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 54:359–369

    Google Scholar 

  • Fernández-Duque E, Erkert HG (2006) Cathemerality and lunar periodicity of activity rhythms in owl monkeys of the Argentinian Chaco. Folia Primatol 77:123–138

    PubMed  Google Scholar 

  • 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:e12572

    PubMed Central  PubMed  Google Scholar 

  • Ganzhorn JU, Wright PC (1994) Temporal pattern in primate leaf eating: the possible role of leaf chemistry. Folia Primatol 63:203–208

    CAS  PubMed  Google Scholar 

  • Ganzhorn JU, Andrianasolo T, Andrianjazalahatra T et al (2007) Lemurs in evergreen littoral forest fragments. In: Ganzhorn JU, Goodman SM, Vincelette M (eds) Biodiversity, ecology and conservation of the littoral ecosystems of south-eastern Madagascar. Smithsonian Institution Press, Washington, pp 223–235

    Google Scholar 

  • Goodman SM (1994a) The enigma of anti-predator behaviour in lemurs: evidence of a large extinct eagle on Madagascar. Int J Primatol 15:129–134

    Google Scholar 

  • Goodman SM (1994b) Description of a new species of subfossil eagle from Madagascar: Stephanoatus (Aves: Falconiformes) from the deposits of Ampasambazimba. P Biol Soc Wash 107:421–426

    Google Scholar 

  • Grassi C (2002) Sex differences in feeding, height, and space use in Hapalemur griseus. Int J Primatol 23:677–693

  • Grassi C (2006) Variability in habitat, diet, and social structure of Hapalemur griseus in Ranomafana National Park, Madagascar. Am J Phys Anthropol 131:50–63

  • Grassman LI Jr, Tewes ME, Silvy NJ (2005) Ranging, habitat use and activity patterns of binturong Arctictis binturong and yellow-throated marten Martes flavigula in north-central Thailand. Wildl Biol 11:49–57

    Google Scholar 

  • Gursky S (2003) Lunar philia in a nocturnal primate. Int J Primatol 24:351–367

    Google Scholar 

  • Hall MI, Ross CF (2007) Eye shape and activity pattern in birds. J Zool 271:437–444

    Google Scholar 

  • Hall MI, Kamilar JM, Kirk EC (2012) Eye shape and the nocturnal bottleneck of mammals. Proc R Soc Lond B 279:4962–4968

    Google Scholar 

  • 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 191–215

    Google Scholar 

  • Halle S (2006) Polyphasic activity patterns in small mammals. Folia Primatol 77:15–26

    PubMed  Google Scholar 

  • Heldmaier G, Steinlechner S, Ruf T, Wiesinger H, Klingenspor M (1989) Photoperiod and thermoregulation in vertebrates: body temperature rhythms and thermogenic acclimation. J Biol Rhythm 4:251–265

    CAS  Google Scholar 

  • Hill RA, Barrett L, Gaynor D, Weingrill T, Dixon P, Payne H, Henzi SP (2003) Day length, latitude and behavioural (in)flexibility in baboons. Behav Ecol Sociobiol 53:278–286

    Google Scholar 

  • 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 266:1127–1132

    CAS  Google Scholar 

  • Horvath JE, Weisrock DV, Embry SL, Fiorentino I, Balhoff JP, Kappeler PM, Wray GA, Willard HF, Yoder AD (2008) Development and application of a phylogenomic toolkit: resolving the evolutionary history of Madagascar’s lemurs. Genome Res 18:489–499

  • Jahn E (1982) Studies on the attack on spruce trees by bark beetles in connection with moon phase. Anz Schadlingskd Pfl 55:145–149

    Google Scholar 

  • Jetz W, Steffen J, Linsenmair KE (2003) Effects of light and prey availability on nocturnal, lunar and seasonal activity of tropical nightjars. Oikos 103:627–639

    Google Scholar 

  • Julien-Laferriere D (1997) The influence of moonlight on activity of woolly opossums (Caluromys philander). J Mammal 78:251–255

    Google Scholar 

  • 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

    Google Scholar 

  • Kaufman DW, Kaufman GA (1982) Effect of moonlight on activity and microhabitat use by Ords’ kangaroo rat (Dipodomys ordii). J Mammal 63:309–312

    Google Scholar 

  • Kerfoot WB (1967) The lunar periodicity of Sphecodogastra texana, a nocturnal bee (Hymenoptera: Halictidae). Anim Behav 15:479–486

    CAS  PubMed  Google Scholar 

  • Kirk EC (2004) Comparative morphology of the eye in primates. Anat Rec 281A:1095–1103

  • Kirk EC (2006) Eye morphology in cathemeral lemurids and other mammals. Folia Primatol 77:27–49

    PubMed  Google Scholar 

  • LaFleur M, Sauther M, Cuozzo F, Yamashita N, Youssouf IAJ, Bender R (2014) Cathemerality in wild ring-tailed lemurs (Lemur catta) in the spiny forest of Tsimanampetsotsa National Park: camera trap data and preliminary behavioral observations. Primates 55:207–217

    Google Scholar 

  • Lang AB, Kalko EKV, Romer H, Bockholdt C, Dechmann DKN (2006) Activity levels of bats and katydids in relation to the lunar cycle. Oecologia 146:659–666

    PubMed  Google Scholar 

  • Martin RD (1972) Adaptive radiation and behaviour of the Malagasy lemurs. Philos T Roy Soc B 264:320–352

    Google Scholar 

  • Mills AM (1986) The influence of moonlight on the behavior of goatsuckers (Caprimulgidae). Auk 103:370–378

    Google Scholar 

  • Morrison DW (1978) Lunar phobia in a Neotropical fruit bat, Artibeus jamaicensis (Chiroptera, Phyllostomidae). Anim Behav 26:852–855

    Google Scholar 

  • 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 221–239

    Google Scholar 

  • Nash LT (1986) Influence of moonlight level on calling and traveling patterns in two sympatric species of Galago in Kenya. In: Taub DM, King FA (eds) Current perspectives in primate social dynamics. Van Nostrand Reinhold, New York, pp 357–367

    Google Scholar 

  • 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 173–205

    Google Scholar 

  • Nievergelt CM, Mutschler T, Feistner ATC (1998) Group encounters and territoriality in wild Alaotran gentle lemurs (Hapalemur griseus alaotrensis). Am J Primatol 46:251–258

    CAS  PubMed  Google Scholar 

  • O’Farrell MJ (1974) Seasonal activity patterns of rodents in a sagebrush community. J Mammal 55:809–823

    Google Scholar 

  • Ollivier FJ, Samuelson DA, Brooks DE, Lewis PA, Kallberg ME, Komáromy AM (2004) Comparative morphology of the tapetum lucidum (among selected species). Vet Ophthalmol 7:11–22

    CAS  PubMed  Google Scholar 

  • Overdorff DJ (1988) Preliminary report on the activity cycle and diet on the red-bellied lemurs (Eulemur rubriventer) in Madagascar. Am J Primatol 16:143–153

    Google Scholar 

  • 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 Press, New York, pp 61–74

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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:e22285

    PubMed Central  CAS  PubMed  Google Scholar 

  • Parga JA (2011) Nocturnal ranging by a diurnal primate: are ring-tailed lemurs (Lemur catta) cathemeral? Primates 52:201–205

    PubMed  Google Scholar 

  • Pariente GF (1979) The role of vision in prosimian behavior. In: Doyle GA, Martin RD (eds) The study of prosimian behavior. Academic, New York, pp 411–459

    Google Scholar 

  • Peichl L (2005) Diversity of mammalian photoreceptor properties: adaptations to habitat and lifestyle? Anat Rec 287A:1001–1012

  • 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 82:413–420

    Google Scholar 

  • Prugh LR, Golden CD (2014) Does moonlight increase predation risk? Meta-analysis reveals divergent responses of nocturnal mammals to lunar cycles. J Anim Ecol 83:504–514

    Google Scholar 

  • Rakotondravony D, Goodman SM, Soarimalala V (1998) Predation on Hapalemur griseus griseus by Boa manditra (Boidae) in the littoral forest of eastern Madagascar. Folia Primatol 69:405–408

    CAS  PubMed  Google Scholar 

  • Rasmussen MA (1999) Ecological influences on activity cycle in two cathemeral primates, Eulemur mongoz (mongoose lemur) and Eulemur fulvus fulvus (common brown lemur). Ph.D. dissertation, Duke University

  • Rea MS, Figueiro MG, Jones GE, Glander KE (2014) Daily activity and light exposure levels for five species of lemurs at the Duke Lemur Center. Am J Phys Anthropol 153:68–77

    PubMed  Google Scholar 

  • Rode-Margono EJ, Nekaris KAI (2014) Impact of climate and moonlight on a venomous mammal, the Javan slow loris (Nycticebus javanicus Geoffroy, 1812). Contrib Zool 83:217–225

    Google Scholar 

  • Saldaña-Vázquez RA, Munguía-Rosas MA (2013) Lunar phobia in bats and its ecological correlates: a meta-analysis. Mamm Biol 78:216–219

    Google Scholar 

  • Santini-Palka ME (1994) Feeding behaviour and activity patterns of two Malagasy bamboo lemurs, Hapalemur simus and Hapalemur griseus, in captivity. Folia Primatol 63:44–49

    CAS  PubMed  Google Scholar 

  • 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 3:239–247

    Google Scholar 

  • Simons EL, Burney DA, Chatrath PS, Godfrey LR, Jungers WL, Rakotosamimanana B (1995) AMS 14C dates for extinct lemurs from caves in the Ankarana Massif, northern Madagascar. Quat Res 43:249–254

    Google Scholar 

  • Starr C, Nekaris KAI, Leung L (2012) Hiding from the moonlight: luminosity and temperature affect activity of Asian nocturnal primates in a highly seasonal forest. PLoS ONE 7:e36396

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Tan CL (2006) Behavior and ecology of gentle lemurs (genus Hapalemur). In: Gould L, Sauther ML (eds) Lemurs: ecology and adaptation. Springer, New York, pp 369–381

    Google Scholar 

  • Tarnaud L (2006) Cathemerality in the Mayotte brown lemur (Eulemur fulvus): seasonality and food quality. Folia Primatol 77:166–177

    PubMed  Google Scholar 

  • Tattersall I (1982) The primates of Madagascar. Columbia University Press, New York

    Google Scholar 

  • Tattersall I (1987) Cathemeral activity in primates: a definition. Folia Primatol 49:200–202

    Google Scholar 

  • Tattersall I (2006) The concept of cathemerality: history and definition. Folia Primatol 77:7–14

    PubMed  Google Scholar 

  • Tofanelli S, Bertoncini S, Castrì L, Luiselli D, Calafell F, Donati G, Paoli G (2009) On the origin and admixture of Malagasy: new evidence from high resolution analyses of paternal and maternal lineages and implications for admixture mapping. Mol Biol Evol 26:2109–2124

    CAS  PubMed  Google Scholar 

  • Upham NS, Hafner JC (2013) Do nocturnal rodents in the Great Basin desert avoid moonlight? J Mammal 94:59–72

    Google Scholar 

  • 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 241–260

    Google Scholar 

  • van Schaik CP, Kappeler PM (1996) The social system of gregarious lemurs: lack of convergence with anthropoids due to evolutionary disequilibrium? Ethology 102:915–941

    Google Scholar 

  • Vasey N (2000) Niche separation in Varecia variegata rubra and Eulemur fulvus albifrons: I. Interspecific patterns. Am J Phys Anthropol 112:411–431

  • Waeber PO, Hemelrijk CK (2003) Female dominance and social structure in Alaotran gentle lemurs. Behaviour 140:1235–1246

    Google Scholar 

  • Wilson JM, Stewart PD, Ramangason GS, Denning AM, Hutchings MS (1989) Ecology and conservation of the crowned lemur Lemur coronatus at Ankarana, north Madagascar. Folia Primatol 52:1–26

    CAS  PubMed  Google Scholar 

  • Wolfe JL, Summerlin CT (1989) The influence of lunar light on nocturnal activity of the old field mouse. Anim Behav 37:410–414

    Google Scholar 

  • Wright PC (1986) Diet, ranging behavior and activity pattern of the gentle lemur (Hapalemur griseus) in Madagascar. Am J Phys Anthropol 69

  • Wright PC (1989) The nocturnal primate niche in the New World. J Hum Evol 18:635–658

    Google Scholar 

  • Wright PC (1990) Patterns of paternal care in primates. Int J Primatol 11:89–102

    Google Scholar 

  • Wright PC (1999) Lemur traits and Madagascar ecology: coping with an island environment. Yearb Phys Anthropol 42:31–72

    Google Scholar 

Download references

Acknowledgments

This work was carried out under the collaboration agreement 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). 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 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. We are grateful for the generous financial support and field gear provided by the American Society of Primatologists, Conservation International’s Primate Action Fund, IDEAWILD, Mohamed bin Zayed Species Conservation Fund (Project Number: 11253008), Primate Conservation Inc., and the Primate Society of Great Britain/Knowsley Safari Park.

Ethical standards

This study complies with Malagasy and German regulations regarding the ethical treatment of research subjects. All research was carried out under the Accord de Collaboration among the University of Antananarivo and the University of Hamburg. Research protocols were approved and permits authorized by Commission Tripartite of the Direction des Eaux et Forêts de Madagascar (Autorisation de recherché No. 240/12/MEF/SG/DGF/DCB.SAP/SCB du 17/09/2012), adhering to the legal requirements of Madagascar.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. Biozentrum Grindel, Department of Animal Ecology and Conservation, University of Hamburg, 20146, Hamburg, Germany

    Timothy M. Eppley & Jörg U. Ganzhorn

  2. Nocturnal Primate Research Group, Department of Social Sciences, Oxford Brookes University, Oxford, OX3 0BP, UK

    Timothy M. Eppley & Giuseppe Donati

Authors
  1. Timothy M. Eppley
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jörg U. Ganzhorn
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Giuseppe Donati
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Timothy M. Eppley.

Additional information

Communicated by M. A. van Noordwijk

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Eppley, T.M., Ganzhorn, J.U. & Donati, G. Cathemerality in a small, folivorous primate: proximate control of diel activity in Hapalemur meridionalis . Behav Ecol Sociobiol 69, 991–1002 (2015). https://doi.org/10.1007/s00265-015-1911-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-015-1911-3

Keywords

Search

Navigation