Seasonal change of daily motor activity rhythms in Capra hircus
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Giuseppe Piccione, Claudia Giannetto, Stefania Casella, and Giovanni Caola Dipartimento di Scienze Sperimentali e Biotecnologie Applicate, Laboratorio di Cronofisiologia Veterinaria, Facolta` di Medicina Veterinaria, Universita` di Messina, 98168 Messina, Italy (e-mail:
[email protected]). Received 11 October 2007, accepted 18 March 2008. Piccione, G., Giannetto, C., Casella, S. and Caola, G. 2008. Seasonal change of daily motor activity rhythms in Capra hircus. Can. J. Anim. Sci. 88: 351355. To evaluate if seasonal changes in photoperiod and temperature were associated with changes in total daily motor activity we recorded the total daily motor activity of five clinically healthy goats at four different times of the year (vernal equinox, summer solstice, autumn equinox and winter solstice). Goats were housed under natural photoperiod and natural ambient temperature in a 12-m2 sound-proof box equipped with 50 100 cm opening window, which allowed natural ventilation. Total motor activity of each goat was recorded by Actiwatch-Mini† , actigraphy-based data loggers that record a digitally integrated measure of motor activity. Our results show the existence of clear seasonal variations in daily activity rhythms in goats, with the highest daily amount of activity during the vernal equinox (769.21982.56 movements h 1) and the lowest during the winter solstice (401.65961.82 movements h1) (PB 0.0001). There was also a change in the amount of motor activity observed during photophase and scotophase through the year (PB0.0001). The cosine peak (times of the daily peaks) always occurred in the middle of the photoperiods and varied from season to season (pB0.0001). Our data indicate that daily motor activity of goats varies with season. Key words: Daily rhythm, environmental condition, total activity, goat Piccione, G., Giannetto, C., Casella, S. et Caola, G. 2008. Variation saisonnie`re du rythme circadien d’activite´ motrice chez Capra hircus. Can. J. Anim. Sci. 88: 351355. Pour e´valuer si les changements saisonniers de la photope´riode et de la tempe´rature entraıˆ nent une modification de l’activite´ motrice totale durant le jour, les auteurs ont releve´ l’activite´ motrice quotidienne de cinq che`vres saines a` quatre moments durant l’anne´e (e´quinoxe vernal, solstice d’e´te´, e´quinoxe automnal et solstice d’hiver). Les animaux e´taient loge´s sous un e´clairage naturel et a` tempe´rature ambiante dans une pie`ce de 12 m2 insonorise´e, pourvue de feneˆtres de 50 x 100 cm permettant une ae´ration naturelle. L’activite´ motrice de chaque sujet a e´te´ releve´e au moyen de l’enregistreur de donne´es Actiwatch-Mini† , qui prend une mesure nume´riquement inte´gre´e des activite´s motrices. Les re´sultats re´ve`lent l’existence de claires variations saisonnie`res dans le rythme d’activite´ circadien des che`vres, la plus forte activite´ survenant a` l’e´quinoxe vernale (769,21982,56 mouvements par heure) et la plus faible, au solstice d’hiver (401,65961,82 mouvements par heure) (PB0,0001). Le degre´ d’activite´ motrice change aussi pendant la photophase et la scotophase durant l’anne´e (PB0,0001). Le pic cosinus (moment des pics quotidiens) revient constamment au milieu de la photope´riode et varie avec la saison (p B0,0001). Les donne´es indiquent que l’activite´ motrice quotidienne des che`vres varie avec la saison. Mots cle´s: Rythme circadien, conditions environnementales, activite´ motrice totale, che`vre
Plants and animals display a circadian rhythm in which key processes show 24-h periodicity. This periodicity is modulated by the 24-h light/dark cycle (Glass 2001), but daily environmental and artificial temperature changes are also characteristic synchronizing signals for the entrainment of the circadian clock in many organisms (Rensing and Rouff 2002). Such behavioural rhythms play a major role in the ecological relations of a species and form part of its evolutionary adaptation (Aschoff 1958), as well as being an adaptation to seasonal and diurnal variations in environmental factors (Cloudsley-Thompson 1961; Risenhoover 1986). Seasonal differences in the locomotor activity pattern of intact animals kept in constant conditions were found to be associated with systemic differences in both the
free-running period (t) of locomotor rhythms and the length of circadian activity (a) (Foa` et al. 1994). Although daily rhythms of locomotor activity have been documented in a large number of species of mammals such as rodents, rabbits, cats, dogs and sheep (Refinetti 2006), few investigations have been conducted on horses (Gill 1991; Scheibe et al. 1999; Piccione et al. 2008) or goats (Shi et al. 2003). Because it has been demonstrated that the daily and annual organization of activity patterns is peculiar to each species, being modulated by both external and internal factors (Boy and Duncan 1979; Nielsen 1984; Pe´pin et al. 1991), our objective was to investigate if seasonal changes in photoperiod and temperature were associated with changes in total daily motor activity in goats at four different times of the year. 351
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352 CANADIAN JOURNAL OF ANIMAL SCIENCE
MATERIALS AND METHODS Five clinically healthy, non-pregnant female goats (Maltese breed, 290.5 yr old, mean body weight 4092 kg) were used. Goats were housed in Palermo (Italy, lat.38.118N, long. 13.358E) under natural photoperiod and indoor ambient temperature. Animals were housed individually in a 12-m2 soundproof box equipped with 50-cm 100-cm opening windows that allowed natural ventilation. The visual and acoustic isolation of each animal avoided the social entrainment of circadian behavioural rhythms (Davidson and Menaker 2003). The animals were put into the experimental box 30 d before the start of the study to avoid changes in the behaviour and physiology of animals due to fear induced by isolation (Carbonaro et al. 1992). The animals had free access to water from a commercial waterer standing 60 cm above the floor and to goodquality alfalfa hay, that was placed on the floor (90.0% DM, 15.8 CP% DM, 50.4 NDF% DM, 31.6 ADF% DM, 5.8 lignin% DM 2.2 EE% DM). From December 205 to September 2006, total activity of goats was recorded as the result of all movements, which includes different behaviours such as feeding, drinking, walking, grooming, and small movements during sleep (Aschoff 1962), independent of the animal’s position such as lying or standing, for 15 d during the following periods: winter solstice from 2005 Dec. 14 to 28 (sunrise at 06450652, sunset at 17161723); vernal equinox from 2006 Mar. 13 to 27 (sunrise at 05350556, sunset at 18361850), summer solstice from 2006 Jun. 14 to 28 (sunrise at 04110413, sunset at 20012005) and autumnal equinox from 2006 Sep. 15 to 29 (sunrise at 05200532, sunset at 18211843). Thermal and hygrometric records were carried out inside the box for the entire study by means of a data logger (Gemini, UK). The data logger was placed 2 m above the floor and recorded data every hour, which were downloaded every 15 d. Both temperature and humidity varied during the year (vernal equinox: 178C, 128C, 70%; summer solstice: 288C, 238C, 68.5%; autumn equinox: 24.08C, 218C, 71%; winter solstice: 15.58C, 10.58C, 73%; maximum and minimum temperatures and mean humidity, respectively). Actiwatch-Mini† (Cambridge Neurotechnology Ltd., UK), actigraphy-based data loggers that record a digitally integrated measure of motor activity were placed on each goat by means of collars that were accepted without any obvious disturbance (Berger 1993; Piccione et al. 2007b). This activity acquisition system is based on miniaturized accelerometer technologies, currently used for human activity monitoring, but also tested for activity monitoring in small non-human mammals (MunozDelgrado et al. 2004; Mann et al. 2005). ActiwatchMini† utilizes a piezo-electric accelerometer that is set up to record the integration of intensity, amount and duration of movement in all directions. The corresponding voltage produced is converted and stored as an activity count in the memory unit of the Actiwatch-
Mini† . Activity was monitored with a sampling interval of 5 min, the values recorded every 5 min were the mean values of the sum of 32 recordings per second. Actograms, a type of graph commonly used in circadian research to plot activity against time, were produced using Actiwatch Activity Analysis 5.06 (Cambridge Neurotechnology Ltd., UK). Total daily activity, the amount of activity during the photophase (the illuminated segment of a light/dark cycle) and the scotophase (the dark segment of a light/dark cycle), and cosine peak (time of peak activity) were calculated using Actiwatch Activity Analysis 5.06 (Cambridge Neurotechnology Ltd., UK). Two-way analysis of variance (ANOVA) was used for the assessment of the effects due to season and days on the daily amount of activity per 24 h, the amount of activity during photophase, the amount of activity during scotophase and cosine peak (P B0.05 was considered statistically significant). Scheffe´’s test was used for post hoc comparison. A paired Student t-test was used to evaluate statistical differences between photophase and scotophase. Intra- and inter-subject variabilities in the amount of activity were computed as the standard deviations of the means. The standard deviations of the mean of the five goats across five days were used as the measure of intrasubject variability. Likewise, the standard deviations of the means for 5 d across the five subjects were used as the measure of inter-subject variability. Although data from 15 d were available for analysis in each case, only the last 5 d were used in the computation of variability in order to ensure a balanced contrast with the number of subjects. All treatments, housing and animal care were carried out under guidelines for the care and use of laboratory animals established by the Italian Ministero della Salute (D.L. 27/1/1992, n 116) and UE (Directive 86/609/ CEE). RESULTS The goats were primarily diurnal, exhibiting greater activity during the photophase than during the scotophase (photophase: 849.009249.99 movements h1, scotophase: 356.879228.86 movements h1, t299 24.83; p B0.001). The daily amount of activity per 24 h changed during the year (winter: 401.65961.82 movements h1, spring: 769.21982.56 movements h1, summer: 669.37974.57 movements h1, autumn: 549.739140.49 movements h1, F(3,240) 229.33; p B0.0001). The highest daily activity was found during the vernal equinox, whereas the lowest activity levels were found during the winter solstice (pB0.0001). The amount of activity during photophase or during scotophase also changed over the course of the year (photophase: F(3,240) 239.99, p B0.0001; scotophase: F(3,240) 64.40, p B0.0001). The greatest daily activity in the photophase was found during the summer solstice (p B0.0001) and the least activity during the autumn equinox (p B0.0001), while the greatest daily activity in
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PICCIONE ET AL. * ACTIVITY RHYTHMS IN CAPRA HIRCUS
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Fig. 1. Representative actograms of total daily activity records in a goat exposed to natural photoperiodic and thermoperiodic conditions during (a) winter solstice, (b) vernal equinox, (c) summer solstice, (d) autum equinox. Each horizontal line is a record of 1 day’s of activity, and consecutive days are mounted one below the other. Total motor activity recorded during cionsecutive 5 min are indicated by black vertical lines. Grey bars indicate the dark phase of the photoperiod.
the scotophase was found during the vernal equinox (pB0.01) and the least during winter solstice (p B0.01). Figure 1 shows the total daily activity recorded from the same animal in the four different seasons. During the four seasons of the year, total activity was prevalent during the photophase, while during the scotophase there were several activity peaks, mostly with lower intensity and shorter than during the photophase, with several cycles of sleep. These activity peaks were more frequent during the summer solstice than the other seasons (P B0.0001). Also, during the winter solstice and the vernal equinox total, motor activity was concentrated in the photophase, from 0630 to 1730 and from 0700 to 1800, respectively. The cosine peak was similar in different animals (F(4,280) 0.06, p0.99), but varied from season to season (F(3,280) 26.88, p B0.0001). The cosine peak occurred between 1230 and 1415 in the winter solstice, between 1230 and 1425 in the vernal equinox, between 1400 and 1700 in the summer solstice and between 1240 and 1645 in the autumn equinox.
Figure 2 shows the intra- and inter-subject variability of total activity during the different seasons. Both interand intra-subject variabilities were higher in the autumn
Fig. 2. Results of the analysis of inter-subject and intra-subject variablility of total daily motor activity during four different seasons. Each bar corresponds to the mean of five animals (9 SEM). Dark bars refer to inter-subject variability and clear bars to intra-subject variability.
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than in the other seasons (F(3,24) 8.05, p 0.001n), but there was no significant effect of variability type per se (F(1,8) 0.047, p0.10) or of their interaction (F(3,24) 0.151, p 0.10). DISCUSSION The results obtained show the existence of clear daily rhythms of activity in goats during the four seasons of the year. In goats, the major grazing periods begin near dawn and recur in late afternoon, ending close to sunset; however, when daylight is short, these two periods merge (Arnold 1985). During ad libitum conditions, water and food consumption occurred throughout the day with a circadian distribution of food and water intake showing peaks at the beginning of the light phase and at the beginning of the dark phase (Rossi et al. 1999). In the present study, the greatest daily activity during the vernal equinox may depend on favourable environmental factors such as ambient temperature; the thermoneutral zone in goats is between 13 and 218C (Martini 1973). The least goat activity during the winter solstice could be related to the shorter photoperiods, the lowest temperatures of the year and environmental factors (Haenlein et al. 1992). The same factors could be implicated in the greatest daily activity in the dark phase during the vernal equinox, and the least daily activity in the dark phase during the winter solstice. In fact, when the ambient temperature is around 108C, as observed during the winter solstice in our study, both the amount of time spent eating and the rate of mastication tend to decrease (Haenlein et al. 1992). Temperatures at night between 7 and 98C have little effect on the pattern of night grazing of sheep in the early morning (Arnold 1982). The highest level of daily activity in the photophase during the summer solstice could be due to the long photoperiod (approximately 15 h), and the increase in volume and frequency of water intake necessary to compensate for the potential rise in evaporative water loss accompanying an increased respiratory rate. In addition, multiple behavioural adaptive mechanisms play a major role, including, but not limited to, the seeking of shade and cooler surfaces (Brosh et al. 1998; Mitlo¨hner et al. 2002). Feral goats increased the percentage of day that they spent feeding and reduced their resting time from summer to autumnwinter in response to the decrease in available daylength and, possibly, the decrease in forage quality and biomass. Feral Rum goats had two or three daily peaks of feeding in summer, but showed no obvious daily feeding peaks in winter, possibly because their percentage of feeding time remained relatively high throughout the daytime in winter (Shi et al. 2003). Circadian analysis of goat activity showed that the cosine peak, the time at which the peak of the rhythm occurs, changed during the year. This result indicated a relationship between the peak of the rhythm and the
time of sunrise, which significantly changes during the year. Furthermore when combined with a light/dark cycle, a temperature cycle usually enhances the amplitude when applied in phase with the light/dark cycle. One of the dual effects of Zeitgeber signals on the organism acts directly, while the other acts by entraining the signal, eventually resulting in the optimal adaptation of the organism to the day/night change in the environment (Rietveld et al. 1993; Redlin 2001). Our previous investigation on sheep demonstrated a strong impact of periodic food availability on the daily rhythms of activity (Piccione et al. 2007a). In conclusion, it is possible to suggest that an endogenous timekeeping system controls the circadian rhythms of total daily motor activity in goats. Our results establish that in goats the activity rhythm reaches its peak in the middle of the day, and show the existence of seasonal variations in daily rhythms of activity in goats exposed to natural environmental conditions. Arnold, G. W. 1982. Some factors affecting the grazing behaviour of sheep in winter in New South Wales. Appl. Anim. Ethol. 8: 119125. Arnold, G. W. 1985. Ingestive behaviour. Pages 183200 in A. F. Fraser, ed. World animal science A. Basic information. Ethology of farm animals. A comprehensive study of the behavioural features of the common farm animals. Elsevier. Tokyo, Japan. Aschoff, J. 1958. Tierische Periodik unter dem Einflub von Zeitgebern. Z. Tierpsychol. 15: 130. Aschoff, J. 1962. Spontane lokomotorische aktivitat. Hand. Zool. 11: 174. Berger, A. 1993. Untersuchungen zum Tagesrhythmus beim Przewalskipferd (Equus prezwalsii Poljakov, 1881) im winter. Diplomarbeit HU-Berlin, Germany. Boy, V. and Duncan, P. 1979. Time-budgets of Camargue horse. Developmental changes in the time-budgets of foals. Behaviour 71: 187201. Brosh, A., Aharoni, Y., Degen, A., Wright, D. and Young, B. 1998. Effects of solar radiation, dietary energy and time of feeding on thermoregulatory responses and energy balance in cattle in hot environment. J. Anim. Sci. 76: 26712677. Carbonaro, D. A., Fried, T. H. and Dellmeier, G. R. 1992. Behavioral and physiological responses of dairy goats to isolation. Physiol. Behav. 51: 297301. Cloudsley-Thompson, J. L. 1961. Rhythmic activity in animal physiology and behaviour. Academic Press, New York, NY. Davidson, A. J. and Menaker, M. 2003. Birds of a feather clock together sometimes: social synchronization of circadian rhythms. Curr. Opin. Neurobiol. 13: 765769. Foa`, A., Monteforti, G., Minutini, L., Innocenti, A., Quaglieri, C. and Flamini, M. 1994. Seasonal changes of locomotor activity patterns in ruin lizards Podarcis sicula. I. Endogenous control by the circadian system. Behav. Ecol. Sociobiol. 34: 267274. Gill, J. 1991. A new method for continuous recording of motor activity in horses. Comp. Biochem. Physiol. A 99: 333341. Glass, L. 2001. Synchronization and rhythmic processes in physiology. Nature 410: 277284. Haenlein, G. F. W., Caccese, R. and Sammeltwitz, P. H. 1992. Goat handbook. Pensylvania State University.
Can. J. Anim. Sci. Downloaded from www.nrcresearchpress.com by MICHIGAN STATE UNIV on 01/27/17 For personal use only.
PICCIONE ET AL. * ACTIVITY RHYTHMS IN CAPRA HIRCUS Mann, T. M., Williams, K. E., Pearce, P. C. and Scott, E. A. 2005. A novel method for activity monitoring in small nonhuman primates. Lab. Anim. 39: 169177. Martini, E. 1973. Fisiologia degli animali domestici. Bologna: Libreria Universitaria. L. Tinarelli, Bologna, Italy. Mitlo¨hner, F., Galyean, M. and McGlone, J. 2002. Shade effects on performance, carcass traits, physiology and behavior of heat stressed feedlot heifers. J. Anim. Sci. 80: 20432050. Munoz-Delgrado, J., Corsi-Cabrera, M., Canales-Espinosa, D., Santillan-Doherty, A. M. and Erket, H. G. 2004. Astronomical and meteorological parameters and rest-activity rhythm in the spider monkey, Ateletes geoffroyi. Physiol. Behav. 83: 101117. Nielsen, E. T. 1984. Relation of behavioural activity rhythms to the changes of day and night: a revision of views. Behaviour 89: 147173. Pe´pin, D., Abegg, C. and Richard, C. 1991. Diurnal activity patterns within female herds of isard around parturition time. Can. J. Zool. 69: 776782. Piccione, G., Bertolucci, C., Caola, G. and Foa`, A. 2007a. Effects of restricted feeding on circadian activity rhythms of sheep a brief report. Appl. Anim. Behav. Sci. 107: 233238. Piccione, G., Grasso, F., Fazio, F., Assenza, A. and Caola, G. 2007b. Influence of different schedules of feeding on daily rhythms of blood urea and ammonia concentration in cows. Biol. Rhythm Res. 38: 133139. Piccione, G., Costa, A., Giannetto, C. and Caola, G. 2008. Daily rhythms of activity in horses housed in different stabling conditions. Biol. Rhythm Res. 39: 7984.
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Redline, U. 2001. Neural basis and biological function of masking by light in mammals: suppression of melatonin and locomotor activity. Chronobiol. Int. 18: 737758. Refinetti, R. 2006. Circadian physiology. 2nd ed. Taylor & Francis Group, Boca Raton, FL. Rensing, L. and Rouff, P. 2002. Temperature effect on entrainment, phase shifting, and amplitude of circadian clocks and its molecular bases. Chronobiol. Int. 19: 807864. Rietveld, W. L., Minors, D. S. and Waterhouse, J. M. 1993. Circadian rhythms and masking: an overview. Chronobiol. Int. 10: 306312. Risenhoover, K. L. 1986. Winter activity patterns of moose in interior Alaska. J. Wildl. Manag. 50: 727734. Rossi, R., Del Prete, E., Rokitzsky, J. and Scharrer, E. 1999. Circadian drinking during ad libitum and restricted feeling in pygmy goats. Appl. Anim. Behav. 61: 253261. Scheibe, K. M., Berher, A., Langbein, J., Streich, W. J. and Eichhorn, K. 1999. Comparative analysis of ultradian and circadian behavioural rhythms for diagnosis of biorhythmic state of animals. Biol. Rhythm Res. 30: 216233. Shi, J., Dunbar, R. I. M., Buckland, D. and Miller, D. 2003 Daytime activity budgets of feral goats (Capra hircus) on the Isle of Rum: influence of season, age, and sex. Can. J. Zool. 81: 803815.
