Endocrine and metabolic consequences of climate change for terrestrial mammals

Journal Pre-proof Endocrine and metabolic consequences of climate change for terrestrial mammals Andrea Fuller, Shane K. Maloney, Dominique Blache, Christine Cooper PII:

S2451-9650(19)30103-6

DOI:

https://doi.org/10.1016/j.coemr.2019.12.003

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COEMR 126

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Current Opinion in Endocrine and Metabolic Research

Received Date: 5 November 2019 Revised Date:

4 December 2019

Accepted Date: 10 December 2019

Please cite this article as: Fuller A, Maloney SK, Blache D, Cooper C, Endocrine and metabolic consequences of climate change for terrestrial mammals, Current Opinion in Endocrine and Metabolic Research, https://doi.org/10.1016/j.coemr.2019.12.003. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2019 Elsevier Ltd. All rights reserved.

1 Endocrine and metabolic consequences of climate change for terrestrial mammals Andrea Fuller1, Shane K. Maloney1,2, Dominique Blache3, Christine Cooper4,5

1

Brain Function Research Group, School of Physiology, University of the Witwatersrand, Medical School, 7 York Road, Parktown, 2193, South Africa. 2 School of Human Sciences, Faculty of Science, The University of Western Australia, 35 Stirling Highway, Crawley, 6009, Western Australia, Australia. 3 School of Agriculture and Environment and UWA Institute of Agriculture, Faculty of Science, The University of Western Australia, 35 Stirling Highway, Crawley, 6009, Western Australia, Australia. 4 School of Molecular and Life Sciences, Curtin University, Perth, 6847, Western Australia, Australia. 5 School of Biological Sciences, Faculty of Science, The University of Western Australia, 35 Stirling Highway, Crawley, 6009, Western Australia, Australia.

Corresponding author: Andrea Fuller, [email protected], +27-11-717-2363 Other author emails: Shane K. Maloney, [email protected] Dominique Blache, [email protected] Christine Cooper, [email protected]

2 1

ABSTRACT

2 3

Climate change will expose mammals to an array of stressors, some new, and some with

4

increased frequency and severity. Those stressors influence endocrine and metabolic

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function, with potential consequences for the survival and persistence of mammalian

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species. Here we review the likely consequences of climate change on the physiological

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function of terrestrial mammals, including direct effects of increasing air temperatures and

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reduced water availability, as well as the indirect effect of reduced or unpredictable food

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supply. Understanding the mechanisms through which function is altered, and the capacity

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for mammals to maintain homeostasis in a changing environment is essential for predicting

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the impact of climate change on mammals and implementing appropriate conservation

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actions.

13 14

Keywords

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thermoregulation, osmoregulation, heat, dehydration, nutrition, homeostasis

16 17

3 18

1. Introduction

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Climate change is exposing terrestrial mammals to heat and aridity more frequently, limiting

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the supply of energy and water, with consequences for the survival and performance of

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mammals. The endocrine system is central to the response of animals to these

23

environmental challenges and the maintenance of homeostasis in different physiological

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systems. We review recent research on how the endocrine systems that are responsible for

25

the maintenance of thermoregulation, osmoregulation, metabolism, and reproduction are

26

affected by heat, reduced water and reduced food availability. Then, we reflect on the value

27

of this knowledge to assess the capacity of terrestrial species to cope with a changing and

28

unpredictable future climate.

29 30

2. Responses to heat

31 32

Mammals will be exposed to a progressively warming climate with more frequent and more

33

extreme heat waves [1]. While increasing ambient temperature can have positive

34

consequences for animals in cold habitats [2], increasing heat load is often detrimental. At

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high environmental temperatures, heat exchange by radiation, convection, and conduction

36

(“dry” routes of heat exchange) imposes a net heat gain (Figure 1), meaning that mammals

37

can lose excess heat and achieve heat balance only via evaporative cooling [3]. Although for

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large mammals the metabolic cost of panting is low and that of sweating negligible [3],

39

regulatory systems need to manage the competing demands of thermoregulation and

40

osmoregulation on water balance (see below). When animals cannot achieve heat balance

41

in hot conditions, body temperature increases; they become hyperthermic. Hyperthermia

42

results in an increase in metabolic rate through the Q10 effect, resulting in an increase in

43

metabolic heat production [4]. Mammals that are chronically exposed to heat, however, can

44

reduce basal heat production via a reduction in circulating thyroid hormone [5]. Indeed, the

45

depression of metabolic rate is a common response to various environmental stressors ([6];

4 46

see below). Hyperthermia can also trigger lethargy, largely through the generation of central

47

fatigue involving changes in dopamine and serotonin levels [7], resulting in reduced activity

48

and consequently reduced heat production [8].

49 50

General endocrine responses to heat stress include an increase in the plasma concentration

51

of glucocorticoids [9], adrenaline, and noradrenaline [10]. The changes in catecholamine

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concentrations provide an index of the level of activation of the autonomic nervous system

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and reflect the initiation of brain pathways that are involved in keeping the milieu interieur

54

within the homeostatic range. There are differences in heat tolerance between species and

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breeds, possibly as a result of differences in circulating glucocorticoids [11]. Brain oxytocin

56

also increases in response to heat exposure [12], at least in sheep, and it has been

57

proposed that oxytocin could play a role in stress resilience [13].

58 59

Reproduction is affected by heat exposure, from the production of gametes, to gestation and

60

care of young [11]. The reproductive axis of mammals is likely to be directly impacted by

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higher air temperatures and more frequent heat waves, but will also be indirectly impacted

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because the axis is sensitive to energy availability (see below). For males, species with

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external testis are impacted by heat stress at all levels of the reproductive axis [11], from a

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decrease in gonadotrophin release from the hypothalamus, to abnormalities of

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spermatogenesis, including damage to the genetic material in the sperm [14]. Ejaculate

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produced after exposure to heat stress has more spermatozoa with abnormal morphology,

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fewer motile sperm, and slower sperm velocity [11,14]. The main source of damage is

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oxidative stress and germ cell apoptosis, accelerated by a decrease in circulating

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gonadotrophins that leads to a decrease in androgen output from the Leydig cells during

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heat exposure [11,14]. In most species the circulating levels of testosterone and

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gonadotrophins are lower during exposure to heat stress.

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For females, hyperthermia reduces episodic secretion of luteinising hormone (LH),

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suppresses the pre-ovulatory surge of LH, and consequently reduces the gonadotrophin-

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dependent growth of follicles. After ovulation, oocytes are heat sensitive [15]. Implantation

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and embryo development are also compromised because heat stress impacts on steroidal

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balance and increases endometrial production and secretion of prostaglandins (PGF2α) that

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can contribute to embryo loss [11]. A reduction in placental function and a decrease in

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progesterone secretion also impairs fetal growth and increases the incidence of teratological

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defects [11,14]. Overall, heat stress decreases fertility because of the combined effect of

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damaged and fragile sperm and oocytes, altered expression of sexual behaviour in both

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sexes because of steroid imbalance, and reduced potential of the oocytes to develop into a

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blastocyst [16].

84 85

3. Responses to reduced water

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To maintain adequate body water in the face of reduced precipitation and increased

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evapotranspiration with climate change, mammals will need to reduce water turnover by

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limiting losses via urine, faeces and evaporation [17]. When water balance is not achieved,

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the reduction in plasma volume and increase in plasma osmolality trigger the secretion of

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antidiuretic hormone (ADH) from the posterior pituitary, resulting in increased permeability of

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renal tubules to water, increased water reabsorption and urinary osmoconcentration. The

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magnitude of endocrine effects on water reabsorption, and the specific form of ADH, varies

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between species, and even individuals, and therefore presumably so too does the

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propensity

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osmoconcentration helps with water balance, it brings the risk, at least in humans in warm

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conditions, of kidney stones [19,20]. It is thought that kidney stones form when fluid

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imbalance results in ADH secretion, urinary concentration, low urine volume and low pH.

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These changes increase the relative supersaturation of calcium and uric acid, thereby

for

species

to

respond

to

changing

water

availability

[18].

While

6 100

promoting the nucleation, growth, and aggregation of lithogenic minerals in urine,

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presumably a process that may occur in other mammals too.

102 103

Another common response of mammals to dehydration is a reduction in evaporative water

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loss [8,21]. In general, maintenance of body water and the functioning of the circulatory

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system is prioritised over the maintenance of body temperature homeostasis [8,22]. Thus,

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dehydration is accompanied by hyperthermia in heat-exposed mammals [23]. The precise

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endocrinological mechanisms that underly the interaction between thermoregulatory and

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osmoregulatory control mechanisms are not fully understood. The activation of

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osmoreceptors in the lamina terminalis inhibits panting in dehydrated mammals, while, at

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least in humans, hypovolaemia appears to inhibit sweating by relaying neural signals from

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arterial baroreceptors to the hypothalamus [8].

112 113

Mammals that are adapted to arid conditions typically have a lower metabolic rate than other

114

mammals, which means that they have a lower heat production and water turnover [22].

115

When they become dehydrated, many species exhibit a further decrease in metabolism [24],

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a change that, at least in the camel, is associated with a decrease in thyroid function and

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circulating thyroid hormone [25].

118 119

A reduction in feed intake is another response to dehydration. The hypothalamus influences

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feeding behaviour and energy balance via the endocrine and neural systems, and more

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directly by solute receptors. There is a negative relationship between plasma osmolality and

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feeding behaviour. This adaptive response prioritises water balance by reducing the volume

123

of digesta, allowing water in the gut to join the body water pool. The change also decreases

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intake of osmolytes from food and limits the thermogenesis that follows feeding [22,26]. The

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change in feeding behaviour results from a reduction in the sensitivity of the paraventricular

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nucleus and lateral hypothalamus to the usual drivers of feeding, resulting in shorter feeding

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bouts [26]. In contrast, when the arid-zone rodent Notomys alexis is water deprived,

7 128

changes in plasma leptin and ghrelin are associated with changes in the expression of

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orexigenic and anorectic neuropeptide genes in the hypothalamus, resulting in an increase

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in feed intake. The changes result in an increase in metabolic rate and an increase in

131

metabolic water production that seems to help water balance [27]. Some desert-adapted

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ungulates also continue to forage when they are dehydrated and may benefit from an

133

increase in the apparent dry matter digestibility that results from slower passage times [28].

134 135

4. Responses to reduced energy availability

136 137

The reduction and unpredictability of food resources associated with climate change will

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impact on the efficiency of survival strategies that have evolved in more predictable

139

environments. These different strategies, from torpor to seasonal breeding, ensure that

140

animals can survive and proliferate by managing their energy balance to maintain

141

homeostatic function, including thermoregulation, and matching energy-intensive activities,

142

like reproduction, to the environmental supply of energy.

143 144

The maintenance of a high metabolic rate and body temperature requires a high energy

145

intake. When food is restricted, a simultaneous reduction in metabolic rate, body

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temperature and activity helps to achieve energy balance. Torpor and hibernation, typically

147

exhibited by small mammals, are the extreme of the spectrum of such energy-saving

148

strategies [29]. Torpor is triggered by a decrease in leptin and triiodothyronine (T3) acting on

149

the hypothalamus, while arousal is driven by a return of normal T3 levels [30], allowing the

150

individual to respond to short-term changes in food availability. Opportunistic torpor also may

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facilitate survival during and after extreme events such as storms, heat waves, and fire,

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which are increasing in frequency and severity with climate change [31]. For long-term

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hibernators, endocrine control relies on an intrinsic timer, which may be fine-tuned by

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photoperiod (via alteration of melatonin levels during the active phase). Mismatches

8 155

between the timing of hibernation and arousal and environmental conditions may occur

156

because of climate change, with considerable fitness costs [32,33].

157 158

While they do not enter torpor, large mammals also respond to food restriction by reducing

159

their energy expenditure and body temperature [23]. A reduction in body temperature during

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periods with low or unpredictable food availability decreases thermoregulatory costs. For

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example, in the wolverine, a 2.7°C decrease in body temperature at -10°C resulted in a 5.5%

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energy saving [34]. Many species of desert mammal have their lowest metabolic rates and

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body temperature in summer when precipitation and food availability are low, and

164

evapotranspiration high [23]. The largest variation in daily body temperature for food-limited

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large mammals was reported for aardvark after a summer drought, with body temperature

166

varying up to 8.6°C over 24h, and dropping as low as 25°C [35]. The lower metabolic rate of

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large mammals with limited food appears to be attributable partly to a decrease in the mass

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of viscera [36].

169 170

Lower food availability as a consequence of climate change likely will have a direct effect on

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reproduction, because all of the steps in the reproductive cycle are sensitive to nutrient and

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energy availability [37]. While a decrease in metabolism and body temperature will help to

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achieve energy balance, heterothermy may be associated with reduced reproductive output,

174

as shown for wild rabbits [38]. The thermoregulatory and reproductive systems are both

175

impacted by changes in energy balance, most likely via leptin and other metabolic hormones

176

such as insulin, IGR-1 and ghrelin, signalling to kisspeptin / neurokinin B / dynorphin (KNDy)

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neurons that can act at all levels of the hypothalamo-pituitary-gonadal axis [39]. The

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combined effect results in a decrease in energy and nutrient availability and a decrease in

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the production of gametes.

180

9 181

In habitats that are highly seasonal, the timing of reproduction is tightly synchronised with

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the timing of food availability. For many mammals, especially those with long gestation

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periods, a combination of endogenous timing and endocrine cues ensures that mating

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occurs at the appropriate time to synchronise birth with peaks in food availability. The

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synchronisation of mating to forecasted environmental changes has been studied in detail,

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especially in sheep. Variations in day length trigger a cascade of neuroendocrine events that

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lead to the activation of gamete production and sexual behaviour [33,40,41]. Climate change

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is resulting in a dissociation between patterns of ambient temperature, rainfall, and

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snowmelt, together with seasonal impacts on plant growth and insect abundance.

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Photoperiod-driven timing of reproduction may no longer be synchronised with optimised

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food availability, resulting in reduced fecundity [33]. The selection that has previously

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occurred for tightly-regulated photoperiodic timing of reproduction may not allow some

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mammals to persist in the face of rapid and ever-growing mismatches in season and

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environmental variables [32].

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5. Conclusion

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The metabolic rate of a mammal is a multivariate factor that impacts fitness [42,43].

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Increasing unpredictability of food and water with climate change may lead to greater

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prevalence of torpor and hibernation in small mammals [43] and hypometabolism in large

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mammals [23], potentially with costs for individuals (e.g., through decreased survival and

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reproduction), and ecosystem functioning. Understanding the plasticity of endocrine-

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mediated changes in metabolism, within and between species, is critical for predicting how

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mammals will respond to climate change and to inform effective management approaches

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[18].

206 207

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Figure legends

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Figure 1: Heat balance in a mammal. Core body temperature depends on the balance

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between heat gain (metabolic heat production or heat gain through convection, conduction

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or exposure to radiant heat), and heat loss (through convection, conduction and radiation,

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and evaporative water loss such as panting and sweating). The direction and rate of heat

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transfer by convection, conduction and radiation depend on the temperature difference

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between the surface of the animal and that of the environment. The circadian rhythm of core

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body temperature, shown here as the original record of 5-min recordings of body

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temperature (blue line) and the associated fitted cosinor (red line), is a result of changes in

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the balance between heat gain and loss.

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Figure 2: Schematic diagram of the biological functions and regulatory mechanisms that

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may be affected by environmental variations associated with climate change. In response to

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changes in ambient temperature and photoperiod (in seasonal animals), hypothalamic

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signals (not included for clarity) control the secretion of pituitary hormones (green) that

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regulate the activity of effector organs (green). In response to the feed-forward control of the

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hypothalamo-pituitary axis, the effectors produce peripheral endocrine signals (orange).

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Endocrine signals are also produced by the digestive tract and adipose tissue in response to

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the ingestion of nutrients and energy. The peripheral endocrine signals retroact (feed back

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control) on the central nervous system (mainly hypothalamus) to synchronise both the feed-

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forward regulation and the expression of food and water intake and sexual behaviour. The

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interactions between these multiple regulatory loops are responsible for the balance

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between osmoregulation, metabolism, thermoregulation, reproduction, and environmental

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resources. Abbreviations: ACTH: adrenocorticotrophic hormone, ADH, antidiuretic hormone,

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Aldo: aldosterone, AP: anterior pituitary, FSH: follicle stimulating hormone, GC:

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glucocorticoids, LH luteinising hormone, OC: optic chiasma, PP; posterior pituitary, SS: sex

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steroids, T3: triiodothyronine, T4: thyroxine, TSH: thyroid-stimulating hormone.

11 236

Acknowledgements

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We thank Caitlin Wyrwoll for the invitation to write this review.

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Conflict of interest statement

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The authors declare that they have no competing interests.

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Author contributions

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All authors contributed to ideas in this review, all authors revised drafts and approved the

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final version.

248 249

Ethics approval

250 251

Not applicable to this review of published work.

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Funding

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This research did not receive any specific grant from funding agencies in the public,

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commercial, or not-for-profit sectors.

257 258

12 259

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rate. Journal of Experimental Biology, 221:jeb166876.

maximise the likely success of, seasonal reproduction, highlighting similarities in the molecules involved in communicating seasonal information, but differences in the tissues which produce, detect and respond to these molecules.

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The authors promote the application of a quantitative genetics framework, the breeder’s equation, to

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451

of metabolic rate plasticity in response to environmental change. Philosophical Transactions

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B, 374:20180180.

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The authors show that individuals within a species differ in the flexibility of their metabolic rates,

assess the evolutionary potential of metabolic rate and to determine why there may be maintenance of variance in metabolic rates within populations.

including the extent to which they can lower metabolism when food is limited and increase the capacity for aerobic metabolism at a high work rate, with potential consequences for responding to climate change.

18 Figure 1

Thermoregulation

Gain

Loss

Metabolic heat Convection

Convection Conduction

Conduction Radiation

Radiation Evaporation

19 Figure 2

Predictable or unpredictable climatic events Food and water availability Hypothalamus OC AP

PP

Water intake

Sexual behaviour

LH FSH

SS

Gonads

TSH

ADH

Nutrient Energy Thyroid T3 T4

Reproduction

ACTH

Feed intake

Metabolism

Adrenal

Kidney

GC Aldo

Digestive tract Liver, Adipose

Osmoregulation Metabolic hormones Leptin, Insulin, IGF-1, GH, Ghrelin

Conflict of interest

Submitted manuscript: Endocrine and metabolic consequences of climate change for terrestrial mammals

Authors: Andrea Fuller, Shane K. Maloney, Dominique Blache, Christine Cooper

The authors hereby declare: Declarations of interest: none