Seasonal variations in locomotor activity rhythm and diurnal activity in the dromedary camel (Camelus dromedarius) under mesic semi-natural conditions

References

• Achaaban MR, Forsling ML, Ouhsine A, Schroter RC 1992. Plasma AVP and water balance in camels subjected to dehydration and rehydration in hot dry and hot humid environments. Proceeding 1st international Camel conference UAE, Dubai, Arab Emirates, 297–299.
   Google Scholar
• Achaaban MR, Schroter RC, Forsling ML, Ouhsine A. 2000. Salt balance in camels subjected to heat stress and water deprivation under two different environmental conditions. J Camel Pract Res. 7:57–62.
   Web of Science ®Google Scholar
• Alagaili AN, Bennett NC, Amor NM, Hart DW. 2020. The locomotory activity patterns of the arid-dwelling desert hedgehog, Paraechinus aethiopicus, from Saudi Arabia. J Arid Environ. 177(2):104141. doi:https://doi.org/10.1016/j.jaridenv.2020.104141
   Google Scholar
• Alagaili AN, Mohammed OB, Bennett NC, Oosthuizen MK. 2013. A tale of two jirds: locomotor activity patterns of the King jird and the Lybian jird from the Arabian Peninsula. J Arid Environ. 88:102–112. doi:https://doi.org/10.1016/j.jaridenv.2012.09.005
   Web of Science ®Google Scholar
• Aschoff J, Fatranska M, Giedke H, Doerr P, Stamm D, Wisser H. 1971. Human circadian rhythms in continuous darkness: entrainment by social cues. Science. 171:213. doi:https://doi.org/10.1126/science.171.3967.213
   PubMed Web of Science ®Google Scholar
• Aubè L, Fatnassi M, Monaco D, Khorchani T, Lacalandra GM, Hammadi M, Padalino B. 2017. Daily rhythms of behavioral and hormonal patterns in male dromedary camels housed in boxes. PeerJ. 5:e3074–e3074. doi:https://doi.org/10.7717/peerj.3074
   PubMed Web of Science ®Google Scholar
• Ben Goumi M, Faye B. 2002. Adaptation du dromadaire à la déshydratation. Science et changements planétaires. Sécheresse. 13(2):121–129. doi:https://doi.org/10.1006/gcen.1993.1045.
   Google Scholar
• Bengoumi M, Riad F, Giry J, de la Farge F, Safwate A, Davicco MJ, Barlet JP. 1993. Hormonal control of water and sodium in plasma and urine of camels during dehydration and rehydration. Gen Comp Endocrinol. 89:378–386. doi:https://doi.org/10.1006/gcen.1993.1045
   PubMed Web of Science ®Google Scholar
• Bertolucci C, Giannetto C, Fazio F, Piccione G. 2008. Seasonal variations in daily rhythms of activity in athletic horses. Anim: An Int J Anim Biosci. 2:1055–1060. doi:https://doi.org/10.1017/S1751731108002267
   PubMed Web of Science ®Google Scholar
• Bothorel B, Barassin S, Saboureau M, Perreau S, Vivien-Roels B, Malan A, Pévet P. 2002. In the rat, exogenous melatonin increases the amplitude of pineal melatonin secretion by a direct action on the circadian clock. Eur J Neurosci. 16:1090–1098. doi:https://doi.org/10.1046/j.1460-9568.2002.02176.x
   Google Scholar
• Bouâouda H, Achâaban MR, Ouassat M, Oukassou M, Piro M, Challet E, El Allali K, Pévet P. 2014. Daily regulation of body temperature rhythm in the camel (Camelus dromedarius) exposed to experimental desert conditions. Physiol Reports. 2:e12151. doi:https://doi.org/10.14814/phy2.12151
   PubMedGoogle Scholar
• Brown JS, Kotler Bp. 2004. Hazardous duty pay and the foraging cost of predation. Ecol Lett. 7:999–1014. doi:https://doi.org/10.1111/j.1461-0248.2004.00661.x
   Web of Science ®Google Scholar
• Castillo-Ruiz A, Paul MJ, Schwartz WJ. 2012. In search of a temporal niche: social interactions. Prog Brain Res. 199:267–280. doi:https://doi.org/10.1016/B978-0-444-59427-3.00016-2.
   PubMed Web of Science ®Google Scholar
• Challet E. 2007. Minireview: entrainment of the suprachiasmatic clockwork in diurnal and nocturnal mammals. Endocrinology. 148:5648–5655. doi:https://doi.org/10.1210/en.2007-0804
   PubMed Web of Science ®Google Scholar
• Charan J, Kantharia ND. 2013 Oct. How to calculate sample size in animal studies? J Pharmacol Pharmacother. 4(4):303–306. PMID: 24250214; PMCID: PMC3826013. doi:https://doi.org/10.4103/0976-500X.119726.
   PubMedGoogle Scholar
• Chiesa JJ, Aguzzi J, García JA, Sardà F, de la Iglesia HO. 2010. Light intensity determines temporal niche switching of behavioral activity in deep-water Nephrops norvegicus (Crustacea: Decapoda). J of Bio Rhythms 25 :277–287 https://doi.org/https://doi.org/10.1177/0748730410376159
   PubMed Web of Science ®Google Scholar
• Cloudsley-Thompson JL. 1961. Rhythmic activity in animal physiology and behaviour. New york: Academic Press.
   Google Scholar
• Daan S, Albrecht U, Van Der Horst GT, Illnerová H, Roenneberg T, Wehr TA, Schwartz WJ. 2001. Assembling a clock for all seasons: are there M and E oscillators in the genes? J Biol Rhythms. 16(105–16):105–116. doi:https://doi.org/10.1177/074873001129001809
   PubMedGoogle Scholar
• Daan S, Aschoff J. 1975. Circadian rhythms of locomotor activity in captive birds and mammals: their variations with season and latitude. Oecologia. 18:269–316. doi:https://doi.org/10.1007/BF00345851
   PubMed Web of Science ®Google Scholar
• Daan S, Spoelstra K, Albrecht U, Schmutz I, Daan M, Daan B, Rienks F, Poletaeva I, Dell’Omo G, Vyssotski A, et al. 2011. Lab mice in the field: unorthodox daily activity and effects of a dysfunctional circadian clock allele. J Biol Rhythms. 26:118–129. doi:https://doi.org/10.1177/0748730410397645
   PubMed Web of Science ®Google Scholar
• Darian-Smith I, Johnson KO. 1977. Temperature sense in the primate. Br Med Bull. 33:143–148. doi:https://doi.org/10.1093/oxfordjournals.bmb.a071414
   PubMed Web of Science ®Google Scholar
• Davimes JG, Alagaili AN, Bertelsen MF, Mohammed OB, Hemingway J, Bennett NC, Manger PR, Gravett N. 2017. Temporal niche switching in Arabian oryx (Oryx leucoryx): seasonal plasticity of 24h activity patterns in a large desert mammal. Physiol Behav. 177:148–154. doi:https://doi.org/10.1016/j.physbeh.2017.04.014
   PubMed Web of Science ®Google Scholar
• Davimes JG, Alagaili AN, Gravett N, Bertelsen MF, Mohammed OB, Ismail K, Bennett NC, Manger PR. 2016. Arabian Oryx (Oryx leucoryx) respond to increased ambient temperatures with a seasonal shift in the timing of their daily inactivity patterns. J Biol Rhythms. 31:365–374. doi:https://doi.org/10.1177/0748730416645729
   PubMed Web of Science ®Google Scholar
• El Allali K, Achaâban M R, Bothorel B, Piro M, Bouâouda H, El Allouchi M, Ouassat M, Malan A, Pévet P. 2013. Entrainment of the circadian clock by daily ambient temperature cycles in the camel (Camelus dromedarius). Am J Physiol Regul Integr Comp Physiol. 304:R1044–1052. doi:https://doi.org/10.1152/ajpregu.00466.2012
   Google Scholar
• El Allali K, Sghiri A, Bouâouda H, Achaâban MR, Ouzir M, Bothorel B, El Mzibri M, El Abbadi N, Moutaouakkil A, Tibary A, et al. 2018. Effect of melatonin implants during the non-breeding season on the onset of ovarian activity and the plasma prolactin in dromedary Camel. Front Vet Sci. 5:44. doi:https://doi.org/10.3389/fvets.2018.00044
   PubMed Web of Science ®Google Scholar
• Farsi H, Achaâban MR, Piro M, Bothorel B, Ouassat M, Challet E, Pévet P, El AK. 2020. Entrainment of circadian rhythms of locomotor activity by ambient temperature cycles in the dromedary camel. Sci Rep. 10:19515. doi:https://doi.org/10.1038/s41598-020-76535-y
   PubMed Web of Science ®Google Scholar
• Farsi H, Harti D, Achaâban MR, Piro M, Ouassat M, Challet E, Pévet P, El Allali K. 2018. Validation of locomotion scoring as a new and inexpensive technique to record circadian locomotor activity in large mammals. Heliyon. 4:e00980–e00980. doi:https://doi.org/10.1016/j.heliyon.2018.e00980
   PubMed Web of Science ®Google Scholar
• Fenn MGP, Macdonald DW. 1995. Use of middens by red foxes: risk reverses rhythms of rats. J Mammal. 76:130–136. doi:https://doi.org/10.2307/1382321
   Web of Science ®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–e12572. doi:https://doi.org/10.1371/journal.pone.0012572
   PubMed Web of Science ®Google Scholar
• Fowler PA, Racey PA. 1990. Daily and seasonal cycles of body temperature and aspects of heterothermy in the hedgehog Eriuaceus europaeus. J Comp Physiol B. 160:299–307. doi:https://doi.org/10.1007/BF00302596
   PubMed Web of Science ®Google Scholar
• García-Allegue R, Lax P, Madariaga AM, Madrid JA. 1999. Locomotor and feeding activity rhythms in a light-entrained diurnal rodent, Octodon degus. Am J Physiol. 277:R523–531. doi:https://doi.org/10.1152/ajpregu.1999.277.2.R523.
   PubMedGoogle Scholar
• Gauthier-Pilters H. 1958. Quelques Observations Sur L’ecologie Et L’ethologie Du Dromadaire Dans Le Sahara Nord-Occidental. Mammalia. 22:140–151. doi:https://doi.org/10.1515/mamm.1958.22.1-4.140
   Google Scholar
• Giovanni C, Stefania C, Claudia G, Giuseppe P. 2010. Daily locomotor activity in five domestic animals. Anim Biol. 60:15–24. doi:https://doi.org/10.1163/157075610X12610595764057
   Web of Science ®Google Scholar
• Gravett N, Bhagwandin A, Sutcliffe R, Landen K, Chase MJ, Lyamin OI, Siegel JM, Manger PR. 2017. Inactivity/sleep in two wild free-roaming African elephant matriarchs – does large body size make elephants the shortest mammalian sleepers? PloS One. 12:e0171903. doi:https://doi.org/10.1371/journal.pone.0171903
   PubMed Web of Science ®Google Scholar
• Hetem RS, Strauss WM, Fick LG, Maloney SK, Meyer LC, Shobrak M, Fuller A, Mitchell D. 2012a. Does size matter? Comparison of body temperature and activity of free-living Arabian oryx (Oryx leucoryx) and the smaller Arabian sand gazelle (Gazella subgutturosa marica) in the Saudi desert. J Comp Physiol B. 182:437–449. doi:https://doi.org/10.1007/s00360-011-0620-0
   PubMed Web of Science ®Google Scholar
• Hetem RS, Strauss WM, Fick LG, Maloney SK, Meyer LCR, Shobrak M, Fuller A, Mitchell D. 2012b. Activity re-assignment and microclimate selection of free-living Arabian oryx: responses that could minimise the effects of climate change on homeostasis? Zoology. 115:411–416. doi:https://doi.org/10.1016/j.zool.2012.04.005
   PubMed Web of Science ®Google Scholar
• Hoogenboom I, Daan S, Dallinga JH, Schoenmakers M. 1984. Seasonal change in the daily timing of behaviour of the common vole, Microtus arvalis. Oecologia. 61:18–31. doi:https://doi.org/10.1007/BF00379084
   PubMed Web of Science ®Google Scholar
• Hut RA, Mrosovsky N, Daan S. 1999. Nonphotic entrainment in a diurnal mammal, the European Ground Squirrel (Spermophilus citellus). J Biol Rhythms. 14:409–420. doi:https://doi.org/10.1177/074873099129000812
   PubMed Web of Science ®Google Scholar
• Hut RA, Pilorz V, Boerema AS, Strijkstra AM, Daan S. 2011. Working for food shifts nocturnal mouse activity into the day. PloS One. 6:e17527. doi:https://doi.org/10.1371/journal.pone.0017527
   PubMed Web of Science ®Google Scholar
• Khalid EA, Achaaban MR, Bothorel B, Piro M, Bouaouda H, Allouchi M, Ouassat M, Malan A, Pevet P. 2013. Entrainment of the circadian clock by daily ambient temperature cycles in the camel (Camelus dromedarius). Am J Physiol Regul Integr Comp Physiol. 304. doi:https://doi.org/10.1152/ajpregu.00466.2012
   Google Scholar
• Khan B, Leteef M, Bilal MQ, Iqbal A, Hassan R. 1998. A study on some of the activity patterns of Camelus dromedarius maintained in Thal area of the Punjab Pakistan. J Pak J Agric Sci. 33:67–72.
   Google Scholar
• Kleitman N, Engelmann TG. 1953. sleep characteristics of infants. Journal of Applied Physiology. 6:269–282. doi:https://doi.org/10.1152/jappl.1953.6.5.269.
   Google Scholar
• Köhler-Rollefson IU. 1991. Camelus dromedarius. Mamm Species. 375:1–8. doi:https://doi.org/10.2307/3504297
   Google Scholar
• Kronfeld-Schor N, Visser ME, Salis L, van Gils JA. 2017. Chronobiology of interspecific interactions in a changing world. Philos Trans R Soc Lond B Biol Sci. 372: 20160248. doi:https://doi.org/10.1098/rstb.2016.0248.
   Google Scholar
• Levy O, Dayan T, Kronfeld-Schor N. 2007. The relationship between the golden spiny mouse circadian system and its diurnal activity: an experimental field enclosures and laboratory study. Chronobiol Int. 24:599–613. doi:https://doi.org/10.1080/07420520701534640
   PubMed Web of Science ®Google Scholar
• Lourens S, Nel JAJ. 1990. Winter activity of bat-eared foxes Otocyon megalotis on the Cape West coast. South African J Zool. 25:124–132. doi:https://doi.org/10.1080/02541858.1990.11448200
   Google Scholar
• McNamara JM. 1987. Starvation and predation as factors limiting population size. Ecology. 68:1515–1519. doi:https://doi.org/10.2307/1939235
   Web of Science ®Google Scholar
• McPhee M, Carlstead K 2010. Effects of Captivity on the Behavior of Wild Mammals. pp. 303–313.
   Google Scholar
• Merrill S, Mech L. 2003. The usefulness of GPS telemetry to study wolf circadian and social activity. Wildl Soc Bull. 31:947–960. doi:https://doi.org/10.2307/3784439
   Web of Science ®Google Scholar
• Metzger J, Wicht H, Korf H-W, Pfeffer M. 2019. Seasonal variations of locomotor activity rhythms in melatonin-proficient and -deficient mice under seminatural outdoor conditions. J Biol Rhythms. 35:58–71. doi:https://doi.org/10.1177/0748730419881922
   PubMed Web of Science ®Google Scholar
• Mrosovsky N, Hattar S. 2005. Diurnal mice (Mus musculus) and other examples of temporal niche switching. J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 191:1011–1024. doi:https://doi.org/10.1007/s00359-005-0017-1
   PubMed Web of Science ®Google Scholar
• Nelson W, Tong YL, Lee JK, Halberg F. 1979. Methods for cosinor-rhythmometry. Chronobiologia. 6:305–323.
   Google Scholar
• Piccione G, Giannetto C, Assenza A, Fazio F, Caola C. 2008a. Locomotor activity and serum tryptophan and serotonin in goats: daily rhythm. J Appl Biomed. 6:73–79. doi:https://doi.org/10.32725/jab.2008.010.
   Google Scholar
• Piccione G, Giannetto C, Casella S, Caola G. 2008b. Circadian activity rhythm in sheep and goats housed in stable conditions. Folia Biologica. 56:133–137. doi:https://doi.org/10.3409/fb.56_3-4.133-137
   PubMed Web of Science ®Google Scholar
• Piccione G, Giannetto C, Casella S, Caola G. 2010. Daily locomotor activity in five domestic animals. Anim Biol. 60:15–24. doi:https://doi.org/10.1163/157075610X12610595764057.
   Web of Science ®Google Scholar
• Pittendrigh CS, Daan SA. 1976. Functional analysis of circadian pacemakers in nocturnal rodents. J Comp Physiol A. 106:33–355. doi:https://doi.org/10.1007/BF01417856
   Google Scholar
• Queiroz MB, Young RJ. 2018. The different physical and behavioural characteristics of zoo mammals that influence their response to visitors. Animals (Basel). 8:139. doi:https://doi.org/10.3390/ani8080139
   Google Scholar
• Refinetti R. 2004. Non-stationary time series and the robustness of circadian rhythms. J Theor Biol. 227:571e581. doi:https://doi.org/10.1016/j.jtbi.2003.11.032
   Web of Science ®Google Scholar
• Refinetti R. 2008. The diversity of temporal niches in mammals. Biol Rhythm Res. 39:173–192. doi:https://doi.org/10.1080/09291010701682690
   Web of Science ®Google Scholar
• Refinetti R, Kaufman CM, Menaker M. 1994. Complete suprachiasmatic lesions eliminate circadian rhythmicity of body temperature and locomotor activity in golden hamsters. J Comp Physiol. 175:223e232. doi:https://doi.org/10.1007/BF00215118
   Web of Science ®Google Scholar
• Riek A, Brinkmann L, Gauly M, Perica J, Ruf T, Arnold W, Hambly C, Speakman JR, Gerken M. 2017. Seasonal changes in energy expenditure, body temperature and activity patterns in llamas (Lama glama). Sci Rep. 7:7600. doi:https://doi.org/10.1038/s41598-017-07946-7
   PubMed Web of Science ®Google Scholar
• Riek A, Stölzl A, Marquina Bernedo R, Ruf T, Arnold W, Hambly C, Speakman JR, Gerken M. 2019. Energy expenditure and body temperature variations in llamas living in the high andes of Peru. Sci Rep. 9:4037. doi:https://doi.org/10.1038/s41598-019-40576-9
   PubMed Web of Science ®Google Scholar
• Saboureau M, Laurent G, Boissin J. 1979. Daily and seasonal rhythms of locomotor activity and adrenal function in male hedgehogs (Erinaceus europaeus L.). Biol Rhythm Res. 10:249–266. doi:https://doi.org/10.1080/09291017909359677.
   Google Scholar
• Schmidt-Nielsen K. 1959. The physiology of the camel. Sci Am Dec. 201:140–151. doi:https://doi.org/10.1038/scientificamerican1259-140. PMID: 14443122.
   PubMed Web of Science ®Google Scholar
• Schmidt-Nielsen K, Schmidt-Nielsen B, Jarnum SA, Houpt TR. 1957. Body temperature of the camel and its relation to water economy. Am J Physiol. 188:103–112. doi:https://doi.org/10.1152/ajplegacy.1956.188.1.103
   PubMed Web of Science ®Google Scholar
• Schumann DM, Cooper HM, Hofmeyr MD, Bennett NC. 2005. Circadian rhythm of locomotor activity in the four-striped field mouse, Rhabdomys pumilio: a diurnal African rodent. Physiol Behav. 85:231–239. doi:https://doi.org/10.1016/j.physbeh.2005.03.024
   PubMed Web of Science ®Google Scholar
• Shkolnik A. 1971. Diurnal activity in a small desert rodent. Int J Biometeorol. 15:115–120. doi:https://doi.org/10.1007/BF01803884
   PubMedGoogle Scholar
• Sih A. 1980. Optimal behavior: can foragers balance two conflicting demands? Science. 210:1041. doi:https://doi.org/10.1126/science.210.4473.1041
   PubMed Web of Science ®Google Scholar
• Tibary A, El Allali K. 2020. Dromedary camel: a model of heat resistant livestock animal. Theriogenology. 15:154–203-211. doi:https://doi.org/10.1016/j.theriogenology.2020.05.046
   Google Scholar
• Touitou Y, Smolensky MH, Portaluppi F. 2006. Ethics, standards, and procedures of animal and human chronobiology research. Chronobiol Int. 23:1083–1096. doi:https://doi.org/10.1080/07420520601055308
   PubMed Web of Science ®Google Scholar
• van der Vinne V, Riede SJ, Gorter JA, Eijer WG, Sellix MT, Menaker M, Daan S, Pilorz V, Hut RA. 2014. Cold and hunger induce diurnality in a nocturnal mammal. Proc National Academy Sci. 111:15256. doi:https://doi.org/10.1073/pnas.1413135111
   PubMed Web of Science ®Google Scholar
• van der Vinne V, Tachinardi P, Riede SJ, Akkerman J, Scheepe J, Daan S, Hut RA. 2019. Maximising survival by shifting the daily timing of activity. Ecology Letters. 22:2097–2102. doi:https://doi.org/10.1111/ele.13404.
   Google Scholar
• Vivanco P, Rol MA, Madrid JA. 2010. Temperature cycles trigger nocturnalism in the diurnal homeotherm Octodon degus. Chronobiol Int. 27:517–534. doi:https://doi.org/10.3109/07420521003743660
   PubMed Web of Science ®Google Scholar
• Vivien-Roels B, Pitrosky B, Zitouni M, Malan A, Canguilhem B, Bonn D, Pévet P. 1997. Environmental control of the seasonal variations in the daily pattern of melatonin synthesis in the European hamster, Cricetus cricetus. Gen Comp Endocrinol, 106: 85–94. doi:https://doi.org/10.1006/gcen.1996.6853
   Google Scholar
• Weinert D, Weinandy R, Gattermann R. 2007. Photic and non-photic effects on the daily activity pattern of Mongolian gerbils. Physiol Behav. 90:325–333. doi:https://doi.org/10.1016/j.physbeh.2006.09.019
   PubMed Web of Science ®Google Scholar
• Wilson RT. 1984. The camel. London: Longman; p. 1–223.
   Google Scholar
• Wu J, Yonezawa T, Kishino H. 2017. Rates of molecular evolution suggest natural history of life history traits and a post-K-Pg nocturnal bottleneck of placentals. Curr Biol: CB. 27:3025–3033.e3025. doi:https://doi.org/10.1016/j.cub.2017.08.043
   PubMed Web of Science ®Google Scholar
• Xue Y, Li J, Sagen G, Zhang Y, Dai Y, Li D. 2018. Activity patterns and resource partitioning: seven species at watering sites in the Altun Mountains, China. J Arid Land. 10:959–967. doi:https://doi.org/10.1007/s40333-018-0028-8
   Web of Science ®Google Scholar
• Yagil R. 1985. The desert Camel. Comp Physiol Adaptation (Comparative animal nutrition). 5:164.
   Google Scholar
• Zhang X. 2015. Molecular sensors and modulators of thermoreception. Channels (Austin). 9:73–81. doi:https://doi.org/10.1080/19336950.2015.1025186
   PubMed Web of Science ®Google Scholar