Shedding light into the dark: Age and light shape nocturnal activity and sleep behaviour of giraffe
Introduction
The behavioural adaptation to internal and external rhythms determines the daily life of an animal. These rhythms are driven by internal circadian clocks, whereby the rhythm of an animal normally oscillates around 24 h, depending on the sunlight (Mistlberger and Rusak, 2011; Partch et al., 2014). The circadian rhythm can be divided into two very different but complementary main states, namely activity and rest (Berger, 2011; Merrow et al., 2005). While active phases are supposed to generate an economic base for the subsequent resting phase, rest is considered as a recovery state gaining new strength for the upcoming challenges of activity (Berger, 2011). Depending on activity peaks within 24 h, species are classified as diurnal, nocturnal, cathemeral or crepuscular (Bennie et al., 2014). With the exception of most large herbivores, the majority of mammals are nocturnal (Wu et al., 2018). However, sleep is extremely diverse in mammals. Regardless of the time of day at which individuals mainly sleep, species can be divided into monophasic (e.g. human and primates) and polyphasic (e.g. rodents, felids or elephants; Phillips et al., 2010) sleepers in terms of length and frequency of sleep events. Most mammals show polyphasic sleep patterns by displaying several fragmented sleep episodes over 24 h (Campbell and Tobler, 1984). In maintaining the daily recurrence of activity and rest, endogenous circadian clocks play just as important a role as external conditions (termed zeitgeber) such as light, temperature or food availability (Berger, 2011; Merrow et al., 2005).
Variations in amount and frequency of specific behavioural patterns over time can be exemplified in activity budgets. The measurement of rest-activity cycles is one of the most applied chronobiological techniques in mammals and birds (Pollak et al., 2001). Within the last decades, daily activity budgets have been studied extensively for several mammal and bird species (Mallapur and Chellam, 2002; Mallapur, 2005; Razal and Miller, 2017; Rees, 2009; Rose and Robert, 2013). Nocturnal behaviour, on the other hand, is still very poorly investigated and understood. Especially in zoos, however, the knowledge of how zoo animals allocate their time during night plays an important role in management and husbandry issues (Brando and Buchanan-Smith, 2018). Behavioural observations including the analyses and generation of activity budgets offer excellent opportunities to close this knowledge gap (Dawkins, 2004; Dawkins, 2006; Fernandez and Timberlake, 2008; Hutchins et al., 2019; Maple, 2007; Maple and Sherwen, 2019) and can serve as a monitoring tool for assessing animal welfare, especially in zoo animals (Hill and Broom, 2009; Hosey et al., 2013; Hutchins et al., 2019; Watters et al., 2009).
There is evidence that the analyses of sensitive behaviour patterns, in particular sleep, can provide these useful information. Previous research on mammals and birds has shown that endogenous processes and biological variables such as age, sex, body size or reproductive state, determine this specific and very sensitive behavioural state just like external stimuli (Ruckstuhl and Neuhaus, 2002 & 2009, Sicks, 2012; Siegel, 2005; Steinmeyer et al., 2010). Sleep in general is thereby defined as a state of immobility with greatly reduced responsiveness (Siegel, 2008). In mammals and birds, this physiological process can be divided into rapid eye movement (REM) and slow wave sleep. During REM sleep, an animal undergoes periodic brain activation partially driven by highly active brainstem neurons as well as localized recuperation processes and emotional regulation. Furthermore, this behavioural state is displayed by specific body posture accompanied by arbitrary muscle twitches (Siegel, 2005 & 2008). Due to this unique body position, this sensitive behaviour is well suited for the analysis of nocturnal activity budgets and possible influencing factors.
Across phylogeny, one of these potential influencing factors is proven to be age (Cajochen et al., 2006; Lesku et al., 2006; Rattenborg et al., 2017; Steinmeyer et al., 2010; Stuber et al., 2015). In most species, activity increases with age and the rest/sleep time decreases within the 24 h cycle. In addition to this and other endogenous variables, exogenous factors also show a significant influence on behaviour (Croft et al., 2016; Berger et al., 2003; Breton and Barrot, 2014; Favreau et al., 2009; Wey et al., 2007). External stimuli thereby may vary from housing conditions to social group constellation aspects or to environmental conditions such as light, sound, food supply or visitor presence. These variables have to be taken into account when assessing potential sources of variation in behaviour (Watters et al., 2009). When analysing behaviour of zoo housed animals, one has to keep in mind that daily staff routines and management processes determine the circadian rhythm of an animal most. Natural dusk and dawn often do not correspond with zoo opening hours and staff time schedules, resulting in shifted day lengths for the animals due to an artificial illuminated enclosure (Brando & Buchannan-Smith 2018). In the course of evolution, animals did not only adapt to spatial but also to temporal niches, leading to changes in species-specific behavioural processes and rhythms (Russart and Nelson, 2018). To ensure survival in a challenging environment while maximizing available resources, individuals optimize their metabolism, physiology and behaviour every day by anticipating and adapting to the daily light-dark cycle (Navara and Nelson, 2007; Russart and Nelson, 2018). Within this adaptation process, light is the most potent oscillator synchronized by the principal pacemaker, the suprachiasmatic nucleus (SCN) of the hypothalamus (Husse et al., 2015; Mistlberger and Rusak, 2011; Moore and Silver, 1998; Reppert and Weaver, 2002). As the absence of light or a permanent exposure to artificial light can cause diseases or even lead to death (Stenvers et al., 2016), recent studies have focused on the impact of light on human and animal behaviour (Fonken and Nelson, 2014; Kirstensen et al., 2007; Navara and Nelson, 2007; Raap et al., 2015; Russart and Nelson, 2018; Stuber et al., 2015; Thomas et al., 2016). The research showed that artificial light impulses during dark phase had a crucial impact on metabolic rate and activity. This presumably strong influence of light must be considered especially for animals living in captivity where they are exposed to artificial light. Beside light, especially feeding routines show high impacts on circadian rhythmicity in mammals (Bloomsmith and Lambeth, 1995; Fernandez and Timberlake, 2008, Gillman et al., 2019; Waitt and Buchanan-Smith, 2001). Since foraging and feeding constitute a large part of the daily activities of most zoo animals (e.g. Rees, 2009; Horback et al., 2014; Razal and Miller, 2017; Veasey et al., 1996) and since this routine is also dominated by human time management, the influence of food and feeding time should be considered when analysing activity budgets.
As one of the four main tasks of modern zoo management is conservation, the activity budget of endangered species is of special interest for ex-situ management aspects (European Association of Zoos and Aquaria, 2014). Regarding the alarming conservation status of giraffe (Giraffa camelopardalis), which was listed vulnerable by the IUCN Red List in 2016, special attention should be paid to this species (Muller et al., 2018). Bearing in mind that the day of a zoo giraffe is determined by staff routines, husbandry activities and visitor presence, it is quite important to pay attention to the hours when animals are not influenced by these factors (Brando and Buchanan-Smith, 2018). This multi-institutional study therefore assessed circadian variation in nocturnal activity and sleep behaviour as well as the influence of light on nocturnal rhythmicity within three different age classes of giraffe. As changes in animal well-being are often associated with changes in behaviour and circadian rhythmicity, the technique of behavioural monitoring used in this study can make a decisive contribution to a better understanding of giraffe baseline behaviours during the night (Watters et al., 2009). The results of this study could serve in a second step as control states against which changes in zoo housed giraffe behaviour can be compared to monitor and improve animal welfare.
Section snippets
Data collection and behavioural states
Data were collected from 63 giraffe (Giraffa camelopardalis) housed at 13 EAZA institutions in Germany and the Netherlands. Giraffe were observed during winter seasons 2015–2018 at Burger’s-Zoo Arnhem, Cologne Zoo, Duisburg Zoo, Erlebniszoo Hannover, Frankfurt Zoo, Münster Zoo, Opel-Zoo Kronberg, Osnabrück Zoo, Schwerin Zoo, Tierpark Berlin, Tierpark Hagenbeck Hamburg, Tiergarten Nuremberg and Zoom Erlebniswelt Gelsenkirchen. Therefore, infrared-sensitive cameras (Mobotix AllRound Dual M15)
Nightly activity budget depending on age classes
We investigated the nightly activity budget (17:00−7:00 h) for three age classes of giraffe for the behaviour patterns feeding, walking, standing, lying and sleeping in REM sleep posture (Table 2). Overall, total amount of resting time differed between the three age classes whereby resting time decreased with increasing age. REM sleep accounted only for 1–3 % per night whereby adults tended to sleep less than juveniles and sub-adults. Total REM sleep time consisted of the number and length of
Nocturnal rhythms
With the results of our study, the nocturnal rhythmicity of activity and REM sleep in captive giraffe could be modelled for the first time and findings provide useful information for husbandry and management. Furthermore, our results confirm previous studies on giraffe’s nightly behaviour (Sicks, 2012; Tobler and Schwierin, 1996) that showed a significant difference in nocturnal activity, REM sleep and rhythmicity depending on age and the length of the dark phase. Thus, analysing nocturnal
Declaration of Competing Interest
The authors declare that they have no competing interests.
Acknowledgement
We gratefully acknowledge support from the directors and curators: Burger’s-Zoo Arnhem, Cologne Zoo, Duisburg Zoo, Erlebniszoo Hannover, Frankfurt Zoo, Münster Zoo, Opel-Zoo Kronberg, Osnabrück Zoo, Schwerin Zoo, Tierpark Berlin, Tierpark Hagenbeck Hamburg, Tiergarten Nuremberg and Zoom Erlebniswelt Gelsenkirchen who enabled this project. A special thanks goes to the zookeepers of the zoos mentioned, who contributed significantly to the success of this study by filling out the questionnaire,
References (101)
- et al.
A survey assessment of variables related to stereotypy in captive giraffe and okapi
Appl. Anim. Behav. Sci.
(2001) - et al.
Effects of predictable versus unpredictable feeding schedules on chimpanzee behaviour
Appl. Anim. Behav. Sci.
(1995) - et al.
The importance of hormonal circadian rhythms in daily feeding patterns: an illustration with simulated pigs
Horm. Behav.
(2017) - et al.
The 24/7 approach to promoting optimal welfare for captive wild animals
Behav. Processes
(2018) - et al.
Influence of enclosure size on the distances covered and paced by captive tigers (Panthera tigris)
Appl. Anim. Behav. Sci.
(2014) Environmental enrichment and cognitive complexity in reptiles and amphibians: concepts, review, and implications for captive populations
Appl. Anim. Behav. Sci.
(2013)- et al.
Animal sleep: a review of sleep duration across phylogeny
Neurosci. Biobehav. Rev.
(1984) - et al.
Fission-fusion dynamics in wild giraffe may be driven by kinship, spatial overlap and individual social preferences
Anim. Behav.
(2013) - et al.
Current directions in animal social networks
Current Opinion in Behavioural Sciences
(2016) - et al.
Birds of a feather clock together – sometimes: social synchronization of circadian rhythms
Curr. Opin. Neurobiol.
(2003)
Circadian entrainment by food and drugs of abuse
Behav. Processes
The effects of predictability in daily husbandry routines on captive Rhesus macaques (Macaca mulatta)
Appl. Anim. Behav. Sci.
Molecular architecture of the mammalian circadian clock
Trends Cell Biol.
The biology of REM sleep
Curr. Biol.
Modelling sexual segregation in ungulates: effects of group size, activity budgets and synchrony
Anim. Behav.
Activity budgets of Rothschild’s giraffe (Giraffa camelopardalis rothschildi Lydekker, 1903) in the “Zoom Erlebniswelt Gelsenkirchen”
Zool. Gart.
Do all animals sleep?
Trends Neurosci. Educ.
Variation in sleep behaviour in freeliving blue tits, Cyanistes caeruleus: effects of sex, age and environment
Anim. Behav.
Sources of intraspecific variation in sleep behaviour of wild great tits
Anim. Behav.
Agreement between different sleep states and behaviour indicators in dairy cows
Appl. Anim. Behav. Sci.
The impact of streetlights on an aquatic invasive species: artificial light at night alters signal crayfish behaviour
Appl. Anim. Behav. Sci.
What time is feeding? How delays and anticipation of feeding schedules affect stump-tailed macaque behavior
Appl. Anim. Behav. Sci.
The role of actigraphy in the study of sleep and circadian rhythms
Am. Acad. Sleep Med. Rev. Paper. Sleep
The structure of social relationships among captive female giraffe (Giraffa camelopardalis)
J. Comp. Psychol.
The effect of increasing dietary fibre on feeding, rumination and oral stereotypies in captive giraffe (Giraffa camelopardalis)
Anim. Welf.
Biogeography of time partitioning in mammals
PNAS
Activity patterns, chronobiology and the assessment of stress and welfare in zoo and wild animals
Int. Zoo Yearb.
Evaluation of living conditions of free-ranging animals by automated chronobiological analysis of behaviour
Behav. Res. Methods, Instrum. Comput.
Nightly selection of resting sites and group behavior reveal antipredator strategies in giraffe
Ecol. Evol.
Age‐related changes in the circadian and homeostatic regulation of human sleep
Chronobiol. Int.
Cosinor –based rhythmometry
Theor. Biol. Med. Model.
Giraffe. Biology, Behavior and Conservation
Seasonal variations in sleep of free-ranging Arabian oryx (Oryx leucoryx) under natural hyperarid conditions
SleepJ
Using behaviour to assess animal welfare
Anim. Welf.
A user’s guide to animal welfare science
Trends Ecol. Evol.
EAZA Standards for the Accommodation and Care of Animals in Zoos and Aquaria
Circadian rhythm, lifestyle and health: a narrative review
Iran J. Public Health
Social influences on circadian behavioural rhythms in vertebrates
Anim. Behav.
Ecology of Desert-dwelling Giraffe Giraffa camelopardalis Angolensis in Northwestern Namibia. Dissertation
Mutual benefits of research collaborations between zoos and academic institutions
Zoo Biol.
Illuminating the deleterious effects of light at night
F1000Med. Reports
The effects of light at night on circadian clocks and metabolism
Endocr. Rev.
BORIS: a free, versatile open-source event-logging software for video/audio coding and live observations
Methods Ecol. Evol.
Circadian rhythm profiles in woman with night eating syndrome
J. Biol. Rhythms
Circadian rhythms of trematode parasites: applying mixed models to test underlying patterns
Parasitology
A brief introduction to mixed effects modelling and multimodel inference in ecology
PeerJ
Measuring zoo animal welfare: theory and practice
Zoo Biol.
Diurnal and nocturnal activity budgets of zoo elephants in an outdoor facility
Zoo Biol.
The first description of dominance hierarchy in captive giraffe: not loose and egalitarian, but clear and linear
PLoS One
Zoo Animals. Behaviour, Management, and Welfare
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