Life Cycle of a Cape Ground Squirrel How Many Babies Do Cape Ground Squirrels Have

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Seasonal Patterns of Trunk Temperature Daily Rhythms in Group-Living Cape Ground Squirrels Xerus inauris

• Michael Scantlebury,
• Marine Danek-Gontard,
• Philip W. Bateman,
• Nigel C. Bennett,
• Mary-Beth Manjerovic,
• Kenneth E. Joubert,
• Jane Thousand. Waterman

10

• Published: Apr 27, 2012
• https://doi.org/10.1371/journal.pone.0036053

Figures

Abstract

Organisms answer to cyclical environmental weather by entraining their endogenous biological rhythms. Such physiological responses are expected to be substantial for species inhabiting arid environments which incur large variations in daily and seasonal ambient temperature (T_a). We measured cadre torso temperature (T_b) daily rhythms of Greatcoat ground squirrels Xerus inauris inhabiting an surface area of Kalahari grassland for six months from the Austral wintertime through to the summertime. Squirrels inhabited two different areas: an exposed flood plain and a nearby wooded, shady area, and occurred in dissimilar social grouping sizes, defined past the number of individuals that shared a sleeping burrow. Of a suite of environmental variables measured, maximal daily T_a provided the greatest explanatory ability for mean T_b whereas sunrise had greatest power for T_b acrophase. There were meaning changes in mean T_b and T_b acrophase over fourth dimension with mean T_b increasing and T_b acrophase becoming before as the season progressed. Squirrels too emerged from their burrows before and returned to them later over the measurement menstruum. Greater increases in T_b, sometimes in excess of five°C, were noted during the beginning hour mail emergence, later which T_b remained relatively constant. This is consistent with observations that squirrels entered their burrows during the mean solar day to 'offload' oestrus. In addition, greater T_b amplitude values were noted in individuals inhabiting the flood plain compared with the woodland suggesting that squirrels dealt with increased ecology variability by attempting to reduce their T_a-T_b gradient. Finally, there were pregnant effects of historic period and group size on T_b with a lower and less variable T_b in younger individuals and those from larger group sizes. These data bespeak that Cape footing squirrels have a labile T_b which is sensitive to a number of abiotic and biotic factors and which enables them to be active in a harsh and variable environment.

Citation: Scantlebury G, Danek-Gontard M, Bateman PW, Bennett NC, Manjerovic M-B, Joubert KE, et al. (2012) Seasonal Patterns of Body Temperature Daily Rhythms in Group-Living Cape Footing Squirrels Xerus inauris. PLoS ONE vii(four): e36053. https://doi.org/10.1371/journal.pone.0036053

Editor: Mark Briffa, University of Plymouth, Great britain

Received: December thirty, 2011; Accustomed: March 26, 2012; Published: April 27, 2012

Copyright: © 2012 Scantlebury et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in whatever medium, provided the original author and source are credited.

Funding: This research was funded by a National Research Foundation Grant IBN0130600 and a Natural Science and Technology Inquiry Council of Canada Discovery Grant to JMW, a National Research Foundation-SAR Chair to NCB and a University of Pretoria PDRF to MS. The funders had no role in study blueprint, data drove and assay, decision to publish, or preparation of the manuscript.

Competing interests: The authors have alleged that no competing interests exist.

Introduction

Organisms respond to cyclical variation in environmental atmospheric condition by entraining their endogenous biological rhythms [one], [two]. Ane such rhythm in endothermic species is that of body temperature (T_b), which is considered to exist a issue of the rest between heat production and estrus dissipation [3]. In many taxa, T_b daily rhythms are influenced by diel and seasonal changes in photoperiod and ambient temperature (T_a) [4]–[9]. Indeed, the primary cues for seasonal acclimatization of the thermoregulatory system, which include changes in T_b daily rhythms, are photoperiod and temperature [ten], [eleven]. Interestingly, lilliputian is known about which selective pressures may impact the evolution of heterothermy in endotherms. Indeed, it is unclear whether one should examine the effects of environmental variation on raw T_b information or utilise some index which can exist comparable beyond species (e.g. 'Heterothermy Index', 'Hi' [12]). Angilletta et al. (2010) [thirteen] suggest that time to come empirical work should examine the potential "selective pressures imposed by regional and temporal heterothermy". They identify several potential candidates which might crusade T_b variations to evolve which include nutrient and water availability, T_a and social huddling. For example, restricted food and water supplies and low T_a values should favor energy-saving reductions in T_b and temporal heterothermy. Implicit in their arguments is the fact that extremes of variation in T_a and in particular cyclical variations in T_a may result in adaptive variation in T_b daily rhythms [xiii]–[sixteen]. For group-living animals, behaviors such as social huddling may be one machinery to conserve water and energy [17], [xviii]. Minimization of thermoregulatory costs and h2o loss are thus seen every bit a possible selective force per unit area for assemblage [19]–[21]. For case, huddling in newborn rabbit (Oryctolagus cuniculus) pups not only saves energy but too affects T_b daily rhythms [22]. Hence, T_b daily rhythms are likely to be afflicted by group size in social animals.

The open up thorn scrub savannah ecosystem of southern Africa is subject to broad diel and annual variations in temperature across seasons, often reaching above 40°C during the summertime and below freezing during the winter [23]. In this habitat, large open areas are interspersed with occasional stands of trees and bushes that generally concentrate in depressions effectually pans and dry river beds [24]. These areas are likely to present unlike microclimatic weather due in office to differences in exposure to solar radiations [25]. Small mammals that inhabit this region, such every bit the Cape ground squirrel (Xerus inauris), exhibit typical arid adaptations including a depression resting metabolic rate, a loftier thermal conductance and a full-bodied urine [26], [27]. They are active twelvemonth-circular and forage during the heat of the day. It has been suggested that they use both behavioral and physiological ways to deal with the extremes of T_a they encounter [28]–[30]. For example, they may be active during hot summertime days considering they periodically dissipate body heat by retreating to libation burrows [31]. Therefore, it is likely that their T_b will vary considerably, both on a daily and a yearly footing, as a physiological adaptation to reduce the T_a-T_b gradient [5], [32], [33]. All the same, information technology is unknown how this is related to microhabitat and behavior, such every bit the time animals emerge in the morning and how they may interact socially with 1 some other.

Here we investigated the role of T_b daily rhythms every bit a response to seasonal and diel changes in T_a in Greatcoat basis squirrels that inhabit a habitat mosaic exposed to large daily and annual temperature fluctuations. Our hypotheses were related to the middle (mesor); the amplitude and the acrophase (time of the peak) of T_b daily rhythms [34]. We predicted that: (a) seasonal differences in T_b daily rhythms would exist apparent with higher mesor values and later on acrophase times during the leap and summer; (b) rapid changes in T_b would exist credible in the early on mornings (later on emergence) and a T_b would be maintained at a constant level throughout the daylight hours considering animals volition move into and out of libation locations such as their burrows as part of their thermoregulatory behavior; (c) lower mesor and aamplitude values of T_b would exist observed in a shaded compared with an open habitat; and (d) winter mesor values would exist college in animals from larger group sizes because of the thermoregulatory benefits gained from huddling at dark. In addition, nosotros examined the potential seasonal variation in HI values from individuals inhabiting unlike locations and from dissimilar group sizes to gauge whether or non relationships that sally when analyzing T_b data are too manifest when using this index.

Materials and Methods

Ethics argument

Permission was granted from South Africa Northwest Parks and Tourism to conduct the field research. The protocol was approved by committee on the ethics of animal experiments of the Universities of Central Florida and Pretoria (permit number UCF IACUC #07-43W). The report was performed in accord with the recommendations in the Guide for the Intendance and Use of Laboratory Animals of the National Institutes of Health.

Animals and report site

Greatcoat ground squirrels are modest (∼600 g), not-hibernating, diurnal, social rodents that inhabit arid regions of sub-Saharan Africa [35]–[37]. They are cooperative breeders with low reproductive skew and a loftier operational sex activity ratio. Groups typically consist of 1–6 related females and their sub adult and juvenile offspring, which share a burrow cluster [35], [38]. The study took place at S. A. Lombard Nature Reserve (three,660 ha, 18 km due north west of Bloemhof, Due south Africa, 27°35′Southward, 25°23′E) as function of an on-going written report where squirrels have been studied since 2002. The site comprises Cymbopogon-Themeda veld and Kalahari grasslands, and is situated on a flood evidently [24]. Mean annual precipitation is 500 mm [39]. Animals were trapped from groups at two locations: an open unshaded area – "the flood plain" – and a habitat containing Acacia karoo and A. erioloba stands – "the woodland", which was approximately 2 km abroad [40]. Tomahawk wire-mesh traps (15×fifteen×50 cm) baited with peanut butter were used to catch animals, after which they were freeze-marked for unique identification (Quick Freeze, Miller-Stephenson Chemical Co., Danbury, CT [41]) and implanted with transponders (PIT tags, Avid Inc., Norco, CA). The sides of animals were as well painted with various shapes using black pilus dye (Rodol D, Lowenstein & Sons Inc., New York, NY) and then their identities could be seen at a distance. Body mass was recorded along with the size of the social groups to which animals belonged. Trapping took place for two ane-week periods during May and October. Age was assessed past knowing dates of kickoff emergence from the natal burrow [35], [42]. Behavioral observations, including times of emergence and immergence from burrows were obtained as outlined in Waterman [37]. Briefly, this involved recording fourth dimension budgets of individual animals by focal sampling in which all-occurrence information were recorded for periods of upwardly to xx minutes whereas the activities of all the individuals inside a group were recorded every 5 minutes past scan sampling [43]. We were interested in many dissimilar aspects, simply in item movement and foraging activities as well equally aggressive, reproductive and social/authorization interactions between individuals.

Acquisition of body temperature (T_b) data

Ten squirrels (five sub adults and five adults) were obtained from the flood evidently and 10 (also five adults and five sub adults) from the woodland. Sub adults are defined as animals between six months subsequently first emergence from the natal burrow and sexual maturity (around viii months for males and nine months for females); adults are individuals which have reached sexual maturity [38]. Miniature temperature recording iButton® dataloggers (DS1922L±0.0625°C; Thermochron, Dallas Semiconductors, Maxim Integrated Products, Inc., Sunnyvale, CA) were surgically implanted into the peritoneal cavity of each individual under anaesthesia (see below). Prior to surgery, devices were calibrated using an APPA 51 digital thermometer in a h2o bath. They were prepare to record every 60 min providing 23 weeks of continuous recordings. Dataloggers were then coated with medical grade surgical wax (ELVAX) [44] and sterilized with formaldehyde vapor. Measurements of T_b were recorded betwixt May 17^th and October 28^thursday 2006.

Squirrels were anaesthetized with medetomidine (Domitor, Pfizer Laboratories (PTY) Ltd, Sandton) (67.vi±ix.2 µg/kg), ketamine (Anaket 5, Centaur Laboratories (PTY) Ltd, Isando) (thirteen.6±1.9 mg/kg) and buprenorphine (Temgesic, Ricketts Laboratories, Isando) (0.five±0.06 µg/kg) [45]. Anesthesia was induced afterwards 3.1±i.4 minutes. The belly was surgically prepared with a chlorhexidine scrub (Hibiscrub, ICL Laboratories), then with chlorhexidine and alcohol (Hibitane, ICI Laboratories). A midline celiotomy was performed for insertion of the dataloggers. The linea alba was airtight with four/0 polydioxanone (PDS, Ethicon, Midrand) and the skin was closed with an intercuticular suture pattern with 4/0 polydioxanone. The procedure for each individual lasted approximately 20 minutes. At the cease of the surgical procedure, anesthesia was reversed with atipamezole (Antisedan, Pfizer Laboratories) (232±92 µg/kg). Recovery occurred within 3.5±2.2 minutes. This procedure was followed for removal of dataloggers for the case of five animals that were recaptured. Three other recaptured animals were euthanized with an overdose of halothane upon recapture as function of a dissimilar study [46]. Only eight of the total xx animals implanted were recaptured. Afterwards removal of dataloggers, T_b data were downloaded using iButton®-TMEX software version three.21 (2004 Dallas Semiconductor MAXIM Corporation). All animals were observed overnight after implantation and removal of dataloggers and returned to their capture site the following morn. No animate being died due to surgical procedures during this period.

Ambient temperature and daylight measurements

Ambient air temperature (T_a) was determined using ii methods. We set dataloggers to record every hour for the offset 84 days (12 weeks) of the sampling period. 1 datalogger was used per study site. Dataloggers were placed within Stevenson screens located ninety cm above the ground. To obtain data over a longer time period, we used daily minimum, maximum and mean ambient temperatures recorded at Bloemhof 27.65 S, 25.60 Due east, GMT +2 (Southward African Weather Agency, Pretoria) for the entire 23 weeks of the sampling period; mean hours of sunlight as well as the times of sunrise (civil dawn) and sunset (civil sunset) were besides noted. In an attempt to measure underground temperatures, we also placed ii dataloggers inside what nosotros idea were disused squirrel burrows. However, these devices did not provide useful information considering the burrows were not vacant; squirrels removed them from the burrows and they were found in spoil heaps on the surface.

Data analyses

Cosinor analysis was used to determine the T_b daily rhythms of the individuals measured [34], [47]. The hateful mesor, amplitude and acrophase values of the T_b daily rhythms were calculated for every individual for each of the 23 weeks of the study period ('T_bmesor', 'T_bamplitude' and 'T_bacrophase', respectively). The significances of the fitted curves were tested against the null hypothesis that the amplitude was zero [48]. The variability in the data that could be accounted for by the fitted curve (percentage rhythm) was calculated. In addition, we calculated the Howdy values for each animal for each week of the study and assessed whether there were whatever relationships between How-do-you-do and flavour, age or group size. Statistical analyses were performed using SPSS 17 (SPSS Inc., Chicago, IL, UsaA.). Mean values are reported ± standard deviations.

(1) Seasonal variation in Tb daily rhythms.

Linear mixed models were used to examine the variation in T_b cosinor parameters (mesor, aamplitude, acrophase) as a office of time (over the 23 week menses). Each dependent variable was analyzed separately. 'Individual ID' was included as a random factor to avoid pseudoreplication and to correct for repeated measurements. 'Week' was included as fixed covariate. As several explanatory terms and their interactions were investigated, models were selected in a stepwise backward fashion, removing the least pregnant explanatory terms until the most parsimonious model was obtained, determined by Akaike's data criterion (AIC). Interaction terms were only included when they were meaning.

(2) Effect of light and ambient temperature (Ta) on body temperature (Tb) daily rhythms.

Linear Mixed Models were used to examine the furnishings of lite and T_a on the mean weekly cosinor parameters. First, we obtained several measures of T_a: the daily minimum (T_amin), the daily maximum (T_amax) and the daily hateful value (T_ahateful) (South African Weather Bureau). We and so calculated weekly averages of T_amin, T_amax and T_amean and included each of these in a model with individual identity as a random gene and week as a fixed effect. This corrected for repeated measurements and differences in mean values between individuals. All potential interactions betwixt temperature variables were included. Models were selected by removing the least significant explanatory terms sequentially until the most parsimonious model was obtained using AIC. Each dependent cosinor variable was analyzed separately. Second, we assessed the effects of various 'calorie-free' variables on the cosinor variable. The light variables we used were: the weekly boilerplate fourth dimension of sunrise, the weekly boilerplate time of dusk and the weekly average length of the photophase. As before, models were selected using AIC by removing to the lowest degree meaning explanatory terms sequentially. Finally, for each of the dependent cosinor variables, combined models were undertaken which included the factors with most explanatory power from both the individual T_a models and the individual low-cal models. Again, for each analysis the best model was obtained using AIC.

(3) Relationship between emergence and immergence times and Tb daily rhythms.

Emergence and immergence times for the two habitats were calculated as the hateful observed emergence and immergence time of groups of squirrels inhabiting both areas [35]. Data were nerveless over vii months of detailed ascertainment time recording when individual squirrel groups from the two habitats emerged or immerged. An boilerplate of 8.i±0.65 squirrels from different groups were observed every week to calculate emergence times and five.7±0.81 squirrels from different groups were observed every calendar week to calculate immergence times. Temporal variation in mean emergence and immergence times was investigated using linear regressions. In gild to determine how daily variations in T_b were related to the times of emergence and whether this differed throughout the year, we computed, for each day, the hateful T_b of each private one hour before the time of emergence and the mean T_b 1 hour later the fourth dimension of emergence. The departure in T_b between these ii values was so calculated every bit a percent of the maximum amplitude difference in T_b for that individual for that twenty-four hours. The mean per centum T_b change for each individual was and so calculated for each week, subsequently which the mean change for all individuals was calculated for the 23 weeks.

(4) Effect of habitat on Ta and Tb daily rhythms.

To examine whether hateful daily T_a differed between the flood evidently and the woodland we conducted linear mixed models with habitat as a fixed gene, calendar week as fourth dimension and T_a measured at both study sites as the dependent variable. To make up one's mind whether high values of T_a obtained during the 24-hour interval or low values obtained during the night differed betwixt the two habitats we included solar day/night as an boosted fixed factor. The hourly T_a obtained at both written report sites were considered equally being 'daytime' T_a if the measurement was taken between the sunrise and sunset of a given twenty-four hours, and 'night-time' T_a if the measure was taken between sunset and sunrise time between two consecutive days. An average T_a was then adamant for each daytime and each night-time period for the 84 days (12 weeks) of the sampling period. To examine the outcome of habitat on hateful weekly T_b values and cosinor parameters, nosotros included 'habitat' and 'twenty-four hour period/night' equally a fixed factors, 'individual' as random variable and 'week' equally cistron.

(5) Upshot of age and group size on Tb daily rhythms.

Effects of age and group size on T_bhateful, T_bmesor, T_bamplitude, T_bacrophase and HI were conducted using linear mixed models with 'individual' as a random variable and 'week' as factor. Models were selected in a stepwise manner using AIC as described previously. Age (adult/sub adult) was included as a chiselled factor and grouping size as a continuous variable.

Results

Of the xx individuals originally implanted with dataloggers, 8 were recaptured; half-dozen from the flood plainly (two adults, four sub adults) and 2 from the woodland (two adults). Group sizes (i.e. the sizes of groups in which the eight animals lived) ranged from one to nine individuals. The implanted animals were regularly observed during the two weeks following implantation and no mortality or immigration was observed. We observed no signs of different beliefs of the implanted squirrels compared to the others. At that place were significant daily rhythms of T_b in all of the eight individuals measured (Tabular array ane, Fig. 1) with hateful ±SD values of the mesor, amplitude and acrophase for the 23 week measurement flow of 37.51±0.15°C, i.thirteen±0.08°C and 12∶33±2 min, respectively.

Effigy ane. Torso temperature (T_b) daily rhythm of an adult Greatcoat ground squirrel (605 g) for the first (21 to 28 May), eighth (09 to 16 July), fifteenth (27 Baronial to 03 September) and twenty-2d week (15 to 22 October) of a 23-week measurement catamenia.

'M' indicates the mesor (37.41°C), 'A' the amplitude (0.92°C) and 'Ø' the acrophase (189.11° or 12∶36 h) of the fitted cosine curve. SR and SS show times of sunrise and dusk.

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Tabular array 1. Mean (±SE) of the mesor (°C), amplitude (°C), acrophase (fourth dimension hh:mm) and percentage rythmicity obtained from 24 h cosine functions of hourly T_b recordings of eight Cape ground squirrels during a 23-week sampling period.

https://doi.org/10.1371/journal.pone.0036053.t001

(1) Seasonal variation in T_b daily rhythms

There were meaning effects of both 'calendar week' and 'individual' on T_bmesor and T_bacrophase (F_i,175 = 35.86, p<0.001 and F_7,175 = viii.51, p<0.001 respectively; Fig. 2A, 2C) indicating that mesor values increased significantly and acrophase values became earlier over the time menses, and that these values differed betwixt individuals. There was also a significant interaction betwixt individual and week on T_bamplitude (F_vii,168 = ii.60, p<0.05; Fig. 2B) indicating that changes in amplitude differed betwixt individuals over time.

Figure 2. Mean ±SE daily rhythm parameters of viii Cape ground squirrels during the 23 week measurement period for: (a) T_b Mesor (°C); (b) T_b Amplitude (°C); (c) T_b Acrophase (time of twenty-four hours and degrees).

Individuals inhabiting the inundation manifestly and the woodland are denoted by solid and open circles. Maximum, minimum and hateful T_a values are shown in (d) as elevation, middle and lower lines.

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(ii) Effect of light and T_a on T_b daily rhythms

Mean T_a values ranged from 7.0±1.4°C during the get-go week to 21.1±0.43°C during the concluding with daily minimum and maximum values of −3°C and 22°C, and nine°C and 36°C respectively (Fig. 2D). By comparing, mean T_b ranged from 37.37±0.11°C during the first week to 37.70±0.12°C during the last. This corresponded to minimum and maximum T_b values of 34.28 and forty.11°C, and 35.64°C and 41.23°C, respectively (Fig. 2A).

When the furnishings of ambience conditions on T_b were examined the simply 'temperature' variable (of T_amin, T_amean and T_amax) that significantly influenced T_bmesor was T_amax (F_ane,60 = 23.87, p<0.001). Similarly, the only 'light' variable that significantly affected T_bmesor was the time of sunset (F_i,99 = 23.72, p<0.001). When both explanatory terms were included into the same model, neither had a meaning effect (p>0.one in both cases). In contrast, although T_amax had a significant effect on T_baamplitude (F_ane,53 = 12.43, p<0.01), T_amean and sunrise were the factors that significantly affected T_bacrophase (F_one,64 = 29.eighty, p<0.001 and F_1,78 = 42.05, p<0.001 respectively), with sunrise being the most important factor in the combined model (F_1,45 = x.90, p<0.01).

(3) Relationships between emergence and immergence times and T_b daily rhythms

Animals emerged afterward in the day at the beginning of the measurement period (07∶44) (May), than at the end (October) (06∶40) (least-squares regression, F_1,46 = 63.25, rⁱⁱ = 0.579, p<0.001). In dissimilarity, immergence times occurred earlier in the 24-hour interval at the beginning of the measurement period (17∶24) than at the end (18∶17) (F_1,45 = 103.02, r^two = 0.696, p<0.001)(Fig. 3). There were no differences in emergence and immergence times between animals that inhabited the inundation plain and the woodland (emergence: F_1,46 = 0.nineteen, p = 0.662; immergence: F_1,45 = 0.17, p = 0.685). However, there was an indication that variation in T_b on a day-by-day basis reflected variation in T_a with depressions in T_b occurring at similar times to depressions in T_a (Fig. iv). Changes in T_b over 24 h periods were greatest at around the times of emergence and immergence, sometimes in excess of v°C, highlighting the potential relationship betwixt T_b and whether or not the animals were higher up or below basis (Fig. 5). During the wintertime (week i), mean increases in T_b for the 60 minutes following emergence were +1.10±0.12°C, which were greater than changes in T_b which occurred in the hour preceding emergence of −0.14±0.xiii°C. During the finish of the measurement menses at week 22, increases in T_b following emergence were less at +0.77±0.12°C compared to +0.48±0.10°C during the hour prior to emergence, respectively. There was a significant departure in the T_b increase between the beginning and the stop of the measurement menses, with a 52% increase in T_b during the first 60 minutes following emergence (relative to the total change in T_b during that twenty-four hour period) during week one and just a corresponding xx% increment in T_b during week 22 (F_1,twenty = 4.99, r² = 0.twenty, p<0.05). T_b values stabilized when animals returned to their burrows in the evening; changes in T_b of −0.01±0.06°C were recorded during the hour post immergence and −0.16±0.06°C during the hour prior to immergence for week 1; this compared to changes of −0.08±0.04°C and −0.20±0.04°C, for postal service-and pre-immergence times during week 22, respectively.

Figure 3. Hateful ±SE immergence and emergence times in the flood plain (solid circles and assuming line) and woodland (open up circles and lite line).

Mean number of animals observed at any one time was 8.1±iv.5 at emergence and 5.6±2.six at immergence.

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Figure 4. T_b (open up circles) and T_a (solid circles) and fitted cosine curves for a Cape ground squirrel during the 9^th week of the sampling catamenia illustrating the variation in T_a and T_b.

The difference betwixt the lowest T_b value recorded (33.39°C at 19:08) and the highest T_b during the previous mean solar day (39.32°C at 16:08) was 5.93°C. Over the 23 week flow, extreme changes in T_b included i individual that decreased in T_b by 5.56°C and another that increased in T_b by 5.98°C in 1 hour.

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Figure v. Mean ±SE T_b changes between successive hours beyond all eight individuals during the first, 8th, fifteenth and twenty-2d weeks of the measurement period.

Gray bars represent the hateful ±SE times of emergence (left-paw bar) and immergence (right-hand bar).

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The mean time at which T_b began to decrease in the mornings across all seasons was 10:thirteen±0:19 minutes and 38.70±0.06°C (Fig. 6). This time became earlier as the measurement catamenia progressed from week ane to week 22. For the weeks 1, viii, 15 and 22, the mean times when T_b commencement decreased were 10:59±0:23, 10:14±0:27, x:22±0:33 and 9:14±0:28 minutes which corresponded to mean T_b values of 38.49±0.07, 38.82±0.eleven, 38.75±0.xiv and 38.72±0.18°C, respectively.

Effigy 6. Mean ±SE T_b of the eight individuals for the get-go, eighth, fifteenth and 20-2nd weeks of the sampling catamenia.

T_b values rose rapidly in the forenoon earlier reaching a plateau during the mean solar day.

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(4) Issue of habitat on T_a and T_b daily rhythms

Mean daily T_a values were not significantly different between the two habitats (F_ane,167 = 0.188, P = 0.665). However, there were pregnant differences between habitats when day and night temperatures were specified in the model (Habitat: F_1,335 = 0.939, p = 0.333; Day/dark: F_1,335 = 1131,p<0.001; Habitat * Solar day/night: F_1,335 = 33.310, p<0.001) indicating that the flood plain was significantly hotter during the day and colder during the night than the woodland. Hateful T_a values in the overflowing evidently were xviii.00±0.41°C during the twenty-four hours and 2.46±0.42°C during the night which compared with values of fifteen.34±0.40°C during the twenty-four hour period and 4.35±0.37°C during the night in the woodland (Fig. 2d).

In that location was a significant effect of habitat on T_bmesor and T_bamplitude values. Values recorded for individuals from the alluvion patently were college than those from the woodland (F_1,150 = x.23, p<0.01 and F_i,159 = 81.58, p<0.001 respectively; Fig. 2A, 2B). Withal, there was no pregnant deviation betwixt T_bacrophase values of individuals from the two habitats (F_1,127 = 1.59, p = 0.210; Fig. 2C).

(5) Effect of age and group size on T_b daily rhythms

At that place were significant interactions between age and body mass on T_bmesor (F_1,111 = 75.eight, p<0.001 respectively). Older individuals decreased T_b with increasing mass whereas T_b was independent of body mass in younger animals. In that location was also a significant effect of group size on T_bmesor with individuals from larger groups having lower T_bmesor values than those from smaller groups (F_1,156 = eighteen.70, p<0.001 respectively; Fig. 7A). There was a significant event of group size (F_i,154 = 22.29, p<0.001) and a meaning interaction betwixt historic period and body mass on T_bamplitude (F_1,153 = 9.22, p = 0.003). Individuals from larger group sizes had lower T_bamplitude values and older animals decreased in T_bamplitude with increasing mass whereas T_baamplitude was contained of body mass in younger animals (Fig. 7B).There were significant interactions betwixt age and body mass and between group size and body mass on T_bacrophase (F_i,74 = 44.26, p<0.001 and F_1,120 = 36.25, p<0.001 respectively; Fig. 7C). Immature animals which were big for their age tended to have T_bacrophase values which occurred earlier in the day whereas larger adults had T_bacrophase values which occurred afterwards. Finally, T_bacrophase values tended to occur later in the twenty-four hours as group size increased but was earliest for a group size of nine.

Figure 7. Mean ±SE values of the mesor, amplitude and acrophase shown per age course (subadults and adults) and for different grouping sizes (1, three, 4, five and 9).

The number of individuals in each category is indicated above the mistake bars. The parameters accept been averaged for the level of private (per category) and then for all weeks, hence SE is non-zero fifty-fifty when merely data from one individual is presented.

https://doi.org/10.1371/journal.pone.0036053.g007

(six) Event of flavour, age and grouping size on the heterothermy index (Hi)

Mean Hullo value across all individuals was 1.23±0.29°C and ranged from 0.68 to 2.32°C. While there were significant differences in Hi values between individuals, in that location was no significant effect of 'week' (F_vii,175 = 22.91, p<0.001 and F_1,175 = 1.fifteen, p = 0.286). However, individuals from larger grouping sizes had lower How-do-you-do values (to the lowest degree squares regression F_one,182 = twenty.33, p<0.001) and there was a meaning interaction between age and group size on HI (F_1,180 = 15.03, p<0.001); older animals decreased in Hullo with increasing group size whereas for immature animals Hello was independent of group size.

Give-and-take

Living in hot barren environments can be stressful for small diurnal mammals since the availability of free water necessary to reduce body heat by evaporation is limited [49]. Consequently, evaporative cooling is oftentimes accompanied by behavioral and physiological mechanisms to misemploy heat such as the use of a thermal refuge or substrate [fifty] or heterothermy [13], [51]–[53]. In the electric current study, Greatcoat ground squirrels were exposed to a wide seasonal and daily range of T_a and the T_bmesor of all individuals increased significantly every bit the flavor progressed. This indicates that T_b values, including both maximal and minimal T_b's were higher on average when T_a values were higher. This volition presumably serve to conserve their water and free energy as a reduced T_a-T_b temperature slope minimizes the need to go on cool by evaporation [15], [54], [55]. In addition, acrophase values became earlier over the measurement period, indicating that activity periods also became earlier [28], [56]. Ground squirrels in full general take labile T_b'southward [2], [five], [57]–[61], T_bamplitudes of different species may vary by iv–5°C and be accompanied past bouts of torpor or hibernation. This compares with T_b amplitude values of up to four.1°C in Arabian oryx (Oryx leucoryx) [51] and 2.6°C in Arabian sand gazelles (Gazella subgutturosa marica) [52]. We found no evidence of torpor and recorded daily variation in T_b, of five–half-dozen°C, which is greater than that noted in virtually other species and greater than noted past Wilson et al. (2010) [33] for Cape ground squirrels in a more than mesic surface area (three.8°C amplitude); hence this probably reflects adaptation to an surround with loftier T_a values and large daily variations in T_a.

(3) Human relationship between T_b daily rhythms, T_a and daylight

Peak ambient temperature (T_amax) was the chief factor that explained both T_bmean and T_bamplitude, which suggests that this is the most thermally challenging menstruum of the twenty-four hours. By comparing, sunrise provided the greatest explanatory power defining T_bacrophase which may suggest that sunrise acted to temporally entrain the thermoregulatory system [62]. Indeed T_bmean increased apace (4–5°C) post-emergence. The sensitivity of organisms to the timing of first calorie-free is exemplified past the fact that calorie-free 'pollution' during the dark stage tin can alter the seasonal acclimation of thermoregulatory, reproductive and immune systems of small mammals [63], [64]. Interestingly, increases in T_b during the starting time hr post-emergence were faster and greater earlier in the measurement period, indicating that animals gained thermal energy more than apace during the winter. This indicates that every bit well equally endogenous rhythms, mechanisms such as sun-basking might also be of import in raising T_b [28], [31], [65], [66]. Whether or non squirrels preferentially orientate themselves to maximize rut uptake whilst basking, for example every bit in Raccoon dogs (Nyctereutes procyonoides) [67], remains unclear. By comparison, subsequently initial increases, the fourth dimension at which T_b stabilized in the mid-morning is likely to be indicative of another regulatory behavior: seeking shelter in burrows or in shade [31], [68]. This effect also became earlier as the season progressed (Fig. seven) suggesting that animals were using thermal refuges to offload rut earlier, allowing periodic bouts of foraging. In that location was also an indication that T_b tracked T_a (Fig. 4) highlighting the thermal lability of these animals. It is probable that Greatcoat ground squirrels were allowing their T_b to vary to defend both water loss and energy expenditure as the greatest amplitudes of variation were noted during the wintertime. Alpine ibex (Capra ibex ibex) also evidence the greatest amplitude of variation of T_b during the winter which the authors suggested promoted a 'thrifty' use of body reserves [9]. By comparing, desert ungulates showed the greatest daily variation in T_b during the summertime (two.6±0.viii°C in Arabian sand gazelles and 4.1±i.7°C in Arabian oryx); this is the season that is near stressful for them when they benefit most by minimizing evaporative water loss [51], [52]. Information technology is noteworthy that T_bmean decreased only before evening immergence and remained steady in one case the squirrels were within their burrows. It seems that the major stimulus to enter burrows could be the prevention of a further decrease in T_b or an increase in energy expenditure due to increased thermoregulation, rather than other possible cues, such as light intensity.

(four) Influence of habitat on T_b daily rhythms

As expected, T_a was more than variable in the flood patently than in the woodland, with the former habitat exhibiting both colder nights and hotter days. Although the sample size was reduced because we were not able to capture many of the individuals that were implanted, the results obtained suggest that T_bamplitude values were besides greater in animals inhabiting the flood plain than the woodland. This may reflect a physiological strategy to minimize the T_a-T_b temperature gradient and save on thermoregulatory costs [55]. In that location were also meaning differences between T_bmesor values of animals inhabiting the two habitats, with higher values recorded in those from the flood plain. This is interesting because T_amesor values did not differ between the two habitats. Therefore, the high T_a experienced during the 24-hour interval must take had a greater outcome on the squirrels' physiology than the T_a experienced during the night in their burrows; moreover the overflowing manifestly was more thermally challenging than the woodland. Presumably squirrels are not exposed to the everyman T_a values during the night considering they shelter in burrows, whereas they are exposed to high T_a values during the mean solar day even though they may use of temporary thermal refuges [68]. This corroborates our previous finding that T_amax held the greatest explanatory power for and T_bmesor.

The fact that variation in physiological characteristics occurred inside a small geographical area suggests that Greatcoat ground squirrels are able to regulate their T_b according to local environmental conditions. Similar patterns have been recorded in other pocket-sized mammals admitting over dissimilar scales. Mutual spiny mouse (Acomys cahirinus) populations a mere two–300 1000 autonomously on either side of a valley in the Mediterranean ecosystem exhibit a suite of physiological differences which include variations in their chronobiology [15], [69], every bit do populations of the broad-toothed field mouse (Apodemus mystacinus) from different sides of the African Great Rift valley [lxx], [71]. A. cahirinus inhabiting a xeric environment had later on T_bacrophase and greater T_bamplitude values than those inhabiting a mesic cooler environment [15]. It was suggested that individuals from the former population immune their T_b to vary considerably, rather than waste water by controlling T_b through evaporation or waste energy using endogenous heat sources, a strategy noted elsewhere [72]–[74]. Since no physical barrier exists betwixt the two sites in the current study, one can assume that there is relatively high within-site fidelity [forty].

(5) Furnishings of age and grouping size on T_b variation

Across taxa, younger animals generally have less prominent T_b daily rhythms than older animals, in part because T_b daily rhythms need time to mature [75], [76]. Larger animals also tend to take smaller T_baamplitude values as a presumed upshot of their greater thermal inertia and reduced susceptibility to changes in food availability [76], [77]. Although our results must be interpreted with caution because of the small sample sizes, these relationships are corroborated every bit a negative correlation was noted between T_bmean and trunk mass in older but not in younger animals. In our instance, heavy young animals also tended to accept earlier T_bacrophase values, indicating earlier activity periods in these individuals. If emergence times are driven by thermoregulatory constraints, information technology is possible that older individuals and those large for their age may emerge earlier because of their lower surface surface area to book ratios and greater thermal capacities. An culling explanation might be that larger animals might just have more fat reserves, allowing them to sally earlier and expend more energy on thermoregulation.

The fact that T_bmesor values decreased with increasing group size suggests that squirrels were expending less energy on thermoregulation in larger groups. Previous studies have suggested that aggregation/huddling behavior tin can significantly reduce thermoregulatory costs [17], [78] and daily averaged energy expenditure [79] in some groups of minor mammals. For example, T_b values were found to be lower in large groups of roosting bats Noctilio albiventris [80]. It was suggested that individual bats in larger groups might be less prone to predation and hence could benefit by lowering their T_b's further than those inside smaller groups. In contrast, for two species of African mole-rat (Cryptomys hottentotus natalensis and Fukomys damarensis), individuals in experimentally increased group sizes had greater T_b values [78]. In this case a crowded burrow which is thermally buffered might go far difficult to cool down and consequently T_b values are greater. Considering Cape footing squirrels fodder during the day as a spaced group [35], any thermoregulatory benefits of grouping size would presumably occur during the night [68] and hence a larger grouping size could facilitate a lower and more stable T_b.

Finally, both T_bamplitude and Hullo were negatively associated with group size and older animals had lower Hello values in larger grouping sizes whereas younger animals did not. This is also consistent with our predictions that individuals in larger groups benefit by being thermally buffered and that older animals are better at regulating their T_b. In this instance, both metrics (T_bamplitude and HI) appear to provide like results, i.e. that there are significant effects of age and group size on T_b variation. Overall, these data confirm that the thermal physiology of Greatcoat footing squirrels is sensitive to changes both in the abiotic and biotic environment. Many factors are observed to touch their T_b, which tin can be modified, enabling them to survive in arid, hostile environments.

Acknowledgments

We would like to give thanks Northwest Parks and Tourism and the staff of S.A. Lombard Nature Reserve for their help and permission to conduct this research. Nosotros would also like to thank Prof. J.Due west. Ferguson for helpful discussions and providing programs to analyse T_b data as well as Justin Boyles and an anonymous reviewer for valuable comments on an earlier draft of the manuscript. Tania Serfontein helped with surgical procedures whilst Lydia Belton, Johannie Caldo, Melissa Hillegass, Tambudzani Mulaudzi, Joe Osbourne and Beth Pettitt provided valuable aid in the field.

Author Contributions

Conceived and designed the experiments: MS. Performed the experiments: MS MBM KEJ. Analyzed the data: MS MDG. Contributed reagents/materials/analysis tools: NCB JMW. Wrote the paper: MS MDG PWB NCB MBM KEJ JMW.

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Source: https://journals.plos.org/plosone/article?id=10.1371%2Fjournal.pone.0036053

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