The locomotory activity patterns of the arid-dwelling desert hedgehog, Paraechinus aethiopicus, from Saudi Arabia

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Highlights

  • Desert hedgehogs from Saudi Arabia entrain their locomotor activity to light cycles

  • They can be described as genuinely nocturnal with an endogenous rhythm.

  • They have free-running rhythms around 24 h

  • Harsh environmental condition decrease behavioural plasticity

  • Global warming may decrease behavioural plasticity in hedgehogs

Abstract

The animal-environment interaction is complex, and the ability to temporally organise locomotor activity provides adaptive and survival advantages. The daily and circadian rhythms of locomotor activity in the Desert hedgehog, Paraechinus aethiopicus, from the central deserts of Saudi Arabia were investigated under controlled laboratory conditions. Twelve individuals were subjected to different light cycles of approximately 3 weeks each: light/dark (12:12LD) cycle; a period of constant darkness (DD); an inverse of the LD (12:12 DL) cycle; a short day cycle (8:16LD); and a long day cycle (16:8LD). All the animals exhibited entrainment of their activity to the LD and DL lighting regimes. Locomotor activity of the Desert hedgehog occurred mostly during the dark phases of the LD, DL, long day and short day cycles. All entraining hedgehogs showed daily rhythmicity, with the periods of the rhythms very close to 24 h. Entrained hedgehogs, additionally, inversed their activity patterns when the light cycle was inversed. The Desert hedgehog, therefore, can be described as genuinely nocturnal with an endogenous rhythm of locomotor activity.

Introduction

Biological clocks are temperature compensated and self-sustaining cellular structures within animals. In mammals, the locations of the internal biological clock is the suprachiasmatic nucleus (SCN), a group of some 10,000 cells (Brady, 1979). The clocks generate biological rhythms that are generated endogenously with a period of close to 24 h and are hence termed circadian rhythms (Stephan and Zucker, 1972; Goldman, 1999; Okamura et al., 2002; Froy, 2007). Circadian rhythms are, subsequently, entrained to a zeitgeber in the natural environment such that the animal can entrain its daily rhythm (synchronized to Earth's 24 h day) to that of the light:dark component of the day or other environmental factors (Stephan and Zucker, 1972; Goldman, 1999; Okamura et al., 2002; Froy, 2007; van Jaarsveld et al., 2019). Biological rhythms are synchronized to cycling external cues, such as the light/dark period (Brady, 1979; Alagaili et al., 2014). In the absence of these entraining factors, biological rhythms free run at their own inherent length, which is slightly different from the normal 24 h cycle of the light: dark cycle experienced in the natural environment. The entrained biological rhythms allow animals to anticipate predictable changes in their environment and thus adjust their behaviour and physiology accordingly which is critical for survival.

One crucial biological rhythm is that of the locomotor activity. The ability of an animal to alter its daily activity during the 24 h day is vital for its survival, as interactions with other animals and environmental conditions at certain times of the day may not be optimal for survival (Lima and Dill, 1990). In many species, such as Gerbillus andersoni, G. pyramidum, Meriones shawi and Dipodillus dasyurus, the predation risk may be higher during the daylight hours in comparison to those of the night (Demas et al., 2001) and environmental conditions, such as temperature, may be elevated during certain times of the 24 h period, this is particularly true in deserts which experience incredibly high temperatures during the day (Alagaili et al., 2013, 2014; 2017; Hart et al., 2018, 2020). Animals may, therefore, adopt diurnal, crepuscular or nocturnal activity patterns to enhance their survival while avoiding harmful conditions (Demas et al., 2001; Alagaili et al., 2012, 2013, 2014).

The majority of species in the family Erinaceidae, which inhabit a wide variety of different habitats, exhibit nocturnal activity patterns, often to avoid diurnal predators in the regions where they occur (DeCoursey et al., 2000; DeCoursey, 2004). For example the Four-toed hedgehog (Atelerix albiventris) (Santana et al., 2010), Long-eared hedgehog (Hemiechinus auritus) (Sharma and Mathur, 1974; Schoenfeld and Yoram, 1985), Daurian hedgehogs (Mesechinus dauuricus) (Zapletal et al., 2012) and southern white-breasted hedgehog (Erinaceus concolor) (Schoenfeld and Yoram, 1985) all have been observed to follow a nocturnal period of activity. However, the strictness to which the nocturnal behaviour is followed varies between species and with season (Sharma and Mathur, 1974; Schoenfeld and Yoram, 1985; Santana et al., 2010; Zapletal et al., 2012). The European hedgehog (E. europaeus) which inhabits the cool and temperate regions of Europe, has been observed to be strictly nocturnal in their activity patterns, with strong entrainment to light (Fowler and Racey, 1990). However, their activity patterns have, additionally, been observed to have seasonal variations, with their nocturnal behaviour being less strictly followed during certain times of the year (Saboureau et al., 1979). During the months of spring and summer (with a characteristically long day photoperiod) European hedgehogs has a strict daily nocturnal locomotor activity behaviour with activity being synchronized with sunset (light off) and sunrise (light on) (Saboureau et al., 1979). Contrastingly, during the months of winter and autumn (short-day photoperiod) their nocturnal behaviour was less strictly followed with activity periods still occurring during the night, but there were no clear relationships with sunset or sunrise (Saboureau et al., 1979).

The majority of small mammals that occur in desert regions have similar behavioural and physiological adaptions to the extreme and harsh environmental conditions that they experience. Small mammals have a large surface area to volume ratio and are thus prone to dehydration and over-heating. As a consequence they must regulate their water and energy balance very efficiently (Macfarlane, 1968). Foraging and other locomotor activities are more advantageous at night when ambient temperatures are cooler, and there is a decrease in the risk of losing water (Macfarlane, 1968; Alagaili et al., 2013, 2014). This nocturnal behaviour seen in desert dwelling small mammals does not preclude predation, as many bird species and other small carnivores also display nocturnal activity; as a consequence it is more likely that the strict nocturnal behaviour exhibited by these desert-dwelling small mammals is in response to extreme daily temperatures (Clements, 2000; Mallon and Budd, 2011).

An under-studied species of hedgehog is the Desert hedgehog, Paraechinus aethiopicus. The Desert hedgehog is widely distributed in the Sahara and the Middle East, such as Saudi Arabia (Harrison and Bates, 1991; He et al., 2012; Alagaili et al., 2017; Boyles et al., 2017). These hedgehogs are found in wadis, around oases and sandy plains where there is vegetation and in agricultural land; they are even known to frequent the coast (Harrison and Bates, 1991). This species of hedgehog is exposed to extreme daily and seasonal environmental conditions, such as long periods of drought, flash floods and extreme daily variation in ambient temperatures with relatively low humidity (Degen, 1997). The Desert hedgehog has consequently adapted to this harsh arid environment. These adaptations include seasonal breeding, with reproduction occurring in early spring and continuing to early summer, which correlates to more accommodating climatic conditions and levels of resources (Al-Musfir and Yamaguchi, 2008; Yamaguchi et al., 2013; Alagaili et al., 2017), hibernation during the cold winters (Al-Musfir and Yamaguchi, 2008) as well as morphological and physiological adjustments to their kidney to decrease water loss in the arid environments they inhabit (Yaakobi and Shkolnik, 1974). The morphological and physiological adjustments to their kidney result in the Desert hedgehog possessing the capabilities of increasing their urine concentration, while under water-restricted experiments, to a much higher concentration in comparison to the European hedgehog and thus indicating a greater ability to conserve water (Yaakobi and Shkolnik, 1974).

Even though the Desert hedgehog has a wide distribution, there is currently a dearth of information pertaining to the activity patterns of this hedgehog species in comparison to other hedgehog species. The Desert hedgehogs used for this study were captured from central Saudi Arabia (Harrison and Bates, 1991), and in comparison to other hedgehog species these study specimens may experience temperatures exceeding 45 °C during the day (in summer), while at night temperatures can drop to as low as −3 °C (in winter). As the effects of climate change, and in particular global warming, begin to be observed, many regions will experience climatic conditions that will drastically change daily temperatures and bring about a decrease in precipitation. This enhanced aridification will have a dramatic effect on animals living in these areas, especially small mammals such as the species of the family Erinaceidae, as the climate has a more significant effect on them due to their smaller body size. An understanding of the behaviour and physiology of these small mammals that inhabit arid regions presently could be pivotal in understanding the possible changes that will arise in other small mammal species which may be faced with future climate extremes. Due to the harsh and challenging conditions, which results in challenges in research, there is a dearth of knowledge in both physiology and behaviour of small mammals that inhabit deserts. In this study, we present baseline knowledge that can be used to assess changes to the activity patterns and behaviour to monitor global warming in the future.

The aim of this study was to assess the locomotory activity pattern of the Desert hedgehog under a number of lighting regimes. It is possible that in future although hedgehogs cue into the light/dark interface, increases in global temperatures may secondarily affect the activity patterns bringing about compression of activity to the cooler periods of the day. The study was conducted to: 1) describe the daily activity pattern of P. aethiopicus under a light/dark cycle; (2) assess whether the Desert hedgehog has an endogenous free running circadian rhythm of locomotory activity under constant lighting conditions and, if so, whether this hedgehog species can entrain the locomotory activity rhythm to a light-dark cycle; (3) calculate the period of the free-running rhythm under constant-dark conditions; 4) to quantitatively describe how activity within the species is distributed over the 24-h day and (5) finally to investigate possible seasonal differences in activity with regard to changing photoperiod (short and long day).

Section snippets

Study site and animal capture

Twelve Desert hedgehogs (Paraechinus aethiopicus) were caught in central Saudi Arabia, in and around the town of Unizah (26.0840° N, 43.9940° E) (Gassim region). The capture sites were predominantly wheat, Alfalfa, Corn and Sorghum farms and desert ecosystem comprising annual grasses, small herbaceous plants, small trees, rocky outcrops and small wadis (Beccari, 1971; Harrison and Bates, 1991; Stone, 1995). Hedgehogs were located at night by using a light beam while driving and then caught by

LD

All Desert hedgehogs under the experimental regimes entrained their locomotory activity rhythms to the light cycle. They showed a preference for locomotory activity during the dark phase of the light cycle, and the majority of the activity occurred during the first part of the night, the first 3 h (Fig. 2, Fig. 3A). The peak activity time for the hedgehogs was after the onset of the dark phase (Figs. 2 and 3A, Table 1). Activity patterns showed clear onsets, while the offset of activity was not

Discussion

The Desert hedgehog under laboratory controlled settings were similar to those experienced by European hedgehogs in the wild, at an ambient temperature of 22 ± 1 °C, desert hedgehogs appeared to restrict locomotor activity to the dark part of the light/dark cycle. The Desert hedgehog entrains its daily locomotor activity to commence after the transition from light to dark and ceases activity as the light comes back on. Very little locomotor activity occurred during the light phase in any of the

Declaration of competing interests

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

The authors extend their appreciation to the International Scientific Partnership Program ISPP at King Saud University for funding this research work through ISPP-123. NCB acknowledges funding from the SARChI chair of Mammalian Behavioural Ecology and Physiology from the DST-NRF South Africa, the National Research Foundation (grant no. 64756), and the University of Pretoria. The research was cleared by the ethics committee of the University of Pretoria.

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