Resilience to Droughts in Mammals: a Conceptual Framework for Estimating Vulnerability of a Single Species

Volume 91, No. 2 THE QUARTERLY REVIEW OF BIOLOGY June 2016

Resilience to droughts in mammals: a conceptual framework for estimating vulnerability of a single species

Tasmin L. Rymer College of Marine & Environmental Sciences and Centre for Tropical Manually chage ligatures Environmental & Sustainability Sciences, James Cook University Cairns, Queensland 4870 Australia School of Animal, Plant & Environmental Sciences, University of the Witwatersrand ﬁ and ﬂ to Johannesburg 2050 South Africa e-mail: [email protected]

ﬁ and ﬂ Neville Pillay School of Animal, Plant & Environmental Sciences, University of the Witwatersrand Johannesburg 2050 South Africa e-mail: [email protected]

Carsten Schradin School of Animal, Plant & Environmental Sciences, University of the Witwatersrand Johannesburg 2050 South Africa Institut Pluridisciplinaire Hubert Curien—Département Ecologie, Physiologie et Ethologie, Université de Strasbourg Strasbourg 67087 France CNRS, UMR7178 Strasbourg 67087 France e-mail: [email protected]

keywords allostasis, homeostasis, metabolism, osmoregulation, preadaptation, thermoregulation

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abstract The frequency and severity of droughts in certain areas is increasing as a consequence of climate change. The associated environmental challenges, including high temperatures, low food, and water availability, have affected, and will affect, many populations. Our aims are to review the behavioral, physiological, and morphological adaptations of mammals to arid environments, and to aid researchers and nature conservationists about which traits they should study to assess whether or not their study species will be able to cope with droughts. We provide a suite of traits that should be considered when making predictions about species resilience to drought. We define and differentiate between general adaptations, specialized adaptations, and exaptations, and argue that specialized adaptations are of little interest in establishing how nondesert specialists will cope with droughts. Attention should be placed on general adaptations of semidesert species and assess whether these exist as exaptations in nondesert species. We conclude that phenotypic flexibility is the most important general adaptation that may promote species resilience. Thus, to assess whether a species will be able to cope with increasing aridity, it is important to establish the degree of flexibility of traits identified in semidesert species that confer a fitness advantage under drying conditions.

Introduction extinct, change their distribution range, or NTHROPOGENIC-induced environ- show an active response to change through Amental change, including habitat adaptive (Breed et al. 2011; Box 1) or exap- loss (Galbraith et al. 2002), fragmentation tive (Ghalambor et al. 2007; Box 1) phe- (Fahrig 2003), and climate change (Et- notypic plasticity. Interestingly, a number terson and Shaw 2001; Alley et al. 2003), of local declines and extinctions due to en- is accelerating at a rate unprecedented in vironmental change have been associated Earth’s history (Etterson and Shaw 2001; with changes in species interactions (Cahill Alley et al. 2003). In fact, the rate of ver- et al. 2013; Ockendon et al. 2014). How- tebrate species climatic niche evolution is ever, an individual’s ability to cope with its considerably slower than the current pre- prevailing environment is also dependent dicted rates of anthropogenic environmen- on its behavior, physiology, and morphol- tal change (Quintero and Wiens 2013). The ogy. These responses to abiotic factors then accelerated rates of human-induced envi- likely also inﬂuence species interactions, ronmental change could thus be driving a for example, through changes in activity sixth mass extinction event, requiring con- patterns, ultimately further impacting ex- servation efforts to be focused on reducing tinction risk. the rate of extinctions (Pimm 2009; Black One of the main consequences of global et al. 2011; Harley 2011). However, we are climate change is an increase in the frequency currently unable to predict which species and intensity of droughts (IPCC 2007; Dai will be threatened by extinction under in- 2011). Regions where droughts have be creased environmental change and which come, and are projected to become, longer species will survive (Moritz and Agudo and more frequent include the Mediterra- 2013). nean, central Europe, central North America, Many studies have assessed the proba- and southern Africa (IPCC 2007). Although bility and potential of species to adapt to the latest IPCC report (2013) mentions a rapid environmental change via evolution- lower conﬁdence for the increased incidence ary adaptation (e.g., evolutionary rescue; of droughts since the 1950s, it is still pre- Gonzalez et al. 2013; Box 1). However, evo dicted that droughts are likely to increase lutionary adaptation is generally a slow in some areas in the future. Droughts are process, occurring over generations (Hoff- a normal part of climate variation, which mann and Sgrò 2011), and may occur too means that, independent of global climate slowly for species to respond to rapid envi change, natural populations have and ronmental and climate change. Under will continue to face this problem repeat- such circumstances, species may become edly. For example, in the last 500 years,

Box 1 Definition of terms Term Definition Adaptive phenotypic plasticity Alteration of some aspect of the phenotype in response to prevailing environmental conditions, which increases an individual’s chance of survival and reproduction (maximizes fitness; Charmantier et al. 2008; Ozgul et al. 2009, 2010; Piersma and van Gils 2010) and that may facilitate population persistence and potentially evolutionary adaptation (Hoffmann and Sgrò 2011). Traits that specifically evolved in response to historical selection pressures and have current utility in the same context (phenotypic adaptation). (100S − 60D) Aridity index Im = ; where Im = index of moisture PEt availability; S = total moisture surplus (mm) from all months with a water surplus; D = total of all monthly deficiencies (mm); and PE = annual potential evapotranspiration (mm; Meigs 1953). Both S and D are represented by the difference between monthly precipitation and monthly potential evapotranspiration (Nash and Engineering Group Work- ing Party 2012). Deserts have an aridity index below 0.2, semideserts between 0.2 and 0.5. Behavioral evader Animals able to escape environmental extremes using primarily behavioral and physiological adaptations (Willmer et al. 2000). Developmental plasticity Nonreversible phenotypic plasticity occurring during ontogeny (Piersma and Lindström 1997). Drought Current precipitation falls significantly below the long-term mean of a defined area (Dai 2011). Is defined on a temporal scale and can occur in any environment. Drought-affected areas Areas that are neither deserts nor semideserts, but experience unpredicted droughts, which might occur more often and become more intense in the future due to climate change (Li et al. 2009). In the future, increasingly more areas might become drought prone due to climate change. Environmental stressor Any stimulus that could affect an individual negatively if it cannot respond to it via a specific stress response, which itself is costly (e.g., Charmandari et al. 2005). Typically uncontrollable for the individual, but can be predictable (e.g., seasonal changes in food) or unpredictable (e.g., a storm; Wingfield 2013).

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Box 1 Continued Term Definition Evolutionary adaptation Change in the relative gene frequencies of alleles (and associated phenotypic changes) within a population over multiple generations, with a corresponding increase in species fitness over time (Pianka 2011; Rezende and Diniz-Filho 2012). Exaptation Formerly called preexisting adaptations or preadaptations. Traits that evolved in response to historical selection pressures, which have current utility but in a different context (i.e., different environment or selection pressures; Gould and Lewontin 1979). Exaptive phenotypic plasticity Alteration of traits in response to prevailing environmental conditions, which specifically evolved in response to historical selection pressures and have current utility in a different context (exaptation), increasing an individual’s chance of survival and reproduction (increasing fitness) in novel environments (Ghalambor et al. 2007). Interannual rainfall variability Expressed as a percentage of the mean deviation of precipitation from the average over the average precipitation (Nash and Engineering Group Working Party 2012). Phenotypic flexibility Reversible phenotypic plasticity (Piersma and Lind- ström 1997). Physiological endurer Animals that tolerate environmental extremes using physiological and morphological adaptations (Willmer et al. 2000). Predictable environment Resources spatially and/or temporally heteroge- neous; selection pressures imposed on populations over multiple generations are seasonal/cyclical (e.g., Negus et al. 1986; Ylönen and Ronkainen 1994); species show evolutionary adaptation and phenotypic plasticity in response to change (Ledón-Rettig et al. 2008; Rymer et al. 2013). Resilience The ability of a species (populations or individuals) to persist following a disturbance or disturbances (Hughes et al. 2007; Tanentzap et al. 2013; Hodg- son et al. 2015). Unpredictable environment Resources spatially and/or temporally heteroge- neous with random, rare, or sporadic environmental changes (Valladares et al. 2002); rapid environment pressure imposed on individuals; and species show phenotypic flexibility in response to change (Piersma and Drent 2003; Rymer et al. 2013). Vulnerability The predisposition or susceptibility of a species (population or individual) to be negatively affected by a disturbance (Smit et al. 2000; Williams et al. 2008; Oppenheimer et al. 2014).

This content downloaded from 137.219.126.019 on May 31, 2016 18:08:34 PM All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c). June 2016 Species Resilience to Droughts 137 megadroughts (extreme drought events adaptive phenotypic plasticity (as per Gha persisting for several years) have occurred lambor et al. 2007) here, although we recognize in North America, China, and West Africa that phenotypic plasticity is not necessar (Dai 2011). ily always adaptive, as the environment can Droughts are characterized by periods of also induce changes that decrease fitness, unusually low water availability due to re- for example, due to constraints or mor- duced precipitation and/or increased evap- phological changes indicating significant oration due to increased temperatures (Dai costs. Another example is evolutionary 2011). Droughts create water shortages, traps, whereby a fitness increasing (“good”) leading to reduced plant primary produc- choice changes into a fitness decreasing tivity (McNaughton et al. 1983) and thus (“poor”) one as previously reliable environ- an associated food reduction for animals, mental cues become unreliable, leading ultimately leading to an increased risk of to an evolutionary mismatch and thereby individual death and population extinction trapping the individual into continuing (Miller et al. 2005; Seager et al. 2007). An- use of the poorer option (Robertson et al. imals exposed to such environmental con- 2013), which could be particularly com- ditions may respond through changes in mon in predictable environments (Box 1). behavior, physiology, and/or morphology Within this context, we argue that whether that facilitate survival and/or reproduc- a trait is specialized and fixed or flexible tion. If individual differences in survival/re- is important for determining the resilience productive probabilities are due to genetic (the ability to persist following a distur- differences, genetic selection within the bance or disturbances; Hughes et al. 2007; population will result in evolutionary ad- Tanentzap et al. 2013; Hodgson et al. 2015) aptation (Rezende and Diniz-Filho 2012). or vulnerability (predisposition or suscepti- Under drought conditions, reproduction bility to be negatively affected by a distur- is often terminated or forfeited, and dry bance; Smit et al. 2000; Williams et al. 2008; seasons are typically the nonbreeding sea- Oppenheimer et al. 2014) of a species (or son (Pinter 1994; Schradin and Pillay 2005; population) to droughts (Box 1). Species Sperry and Weatherhead 2008). Droughts with fixed adaptations to droughts are gen- represent periods of low resource availabil- erally well adapted to arid environments, al- ity that individuals must survive in order to though in species with flexible adaptations reach a season when reproduction again and exaptations, the degree of flexibility becomes possible. For this reason, our fo- determines resilience and will likely facil- cus rests with survival and not on reproduc- itate adaptive evolution in novel environ- tive success. ments (Ghalambor et al. 2007). Resilience Individuals can cope with droughts us- to droughts requires individuals to be able ing a variety of morphological, physiolog- to cope with three environmental stressors: ical, and behavioral traits, and to predict water shortage, food shortage, and fluctu- the extent to which species are resilient to ating (often very high) temperatures. We droughts requires some measure of these define the term “environmental stressor” traits. Here, we review these traits to pro- as any stimulus that could affect an indi- vide researchers and nature conservation- vidual negatively if it cannot respond to it ists with a guide to which phenotypic traits via a specific stress response, which itself should be studied in order to assess whether is costly to some extent. A stress response or not a species of interest may be able to can be an increase in energy mobilization cope with droughts. We describe three dif- (i.e., increased blood glucocorticoid lev- ferent ways species can cope with droughts, els to mobilize energy; Charmandari et al. namely through evolutionary adaptation 2005), but also comprise other physiolog- (future change), adaptive phenotypic plas- ical responses (for example, decrease of ticity (current change), and exaptations blood glucocorticoid levels, if the stressor (including exaptive phenotypic plasticity, is reduced energy availability and the indi- current change). We focus specifically on vidual has to reduce energy mobilization).

Stressors are typically uncontrollable for (e.g., red abalone Haliotis rufescens; de Wit the individual. For example, the individual and Palumbi 2013), and behavior (e.g., cannot control rainfall during a given pe- bird song; Podos et al. 2004). The degree riod. Stressors can occur predictably (e.g., of adaptive phenotypic plasticity also rep- seasonal changes in food) or unpredictably resents an evolutionary adaptation. These (e.g., a storm; Wingfield 2013). adaptations confer a fitness advantage and We then highlight some approaches to evolved in response to particular past se- categorize behavioral, physiological, and lection pressures (Baum and Larson 1991; morphological traits of mammals for ex- Coddington 1994). Evolutionary adaptation istence in deserts and semideserts and in- represents how species responded to previ- troduce our own categorization system, the ous environmental change, and raises the adaptive triquetra, which categorizes traits question of whether, and the degree to facilitating coping with aridity instead of cat- which, species can respond to prevailing egorizing the species themselves. The adap- environmental change via genetic change. tive triquetra system considers the primary Although it is becoming increasingly rec- driving stressor, the body system mounting ognized that evolutionary adaptation can the adaptive response (behavior, physiol- be quite rapid (Hoffmann and Sgrò 2011), ogy, and/or morphology), and the extent the evolutionary response to a changing to which this trait is flexible. We suggest environment can be constrained by a lack that the selection pressures operating in of genetic variation or genetic correlations deserts (defined below) drive the evolu- (i.e., genetic constraints; Chevin 2013), tion of specialized, nonplastic adaptations, the rate at which individuals within a pop- whereas those in semideserts (defined be- ulation reproduce (Lewontin 1970), and low) promote phenotypic flexibility. We also the rate and predictability at which the stress that traits that could potentially facili- strength and direction of selection changes tate future coping (which would be classified (due to environmental change) over time as exaptations) must not be ignored. We (Lande and Shannon 1996; Gomulkiewicz focus our explanation of the adaptive tri- and Houle 2009; Chevin 2013; Michel et al. quetra on mammals, which are one of the 2014). best studied taxa for desert adaptations. Al- Species might not be adapted to prevail- though adaptations in other taxa, such as ing specific environmental pressures, but insects and birds, might be quite different, may still show some degree of resilience to we believe that our general conclusions change due to exaptations, also called pre- would apply to them as well. Finally, we existing adaptations or preadaptations (e.g., conclude that the degree of flexibility of Pekár et al. 2013). In contrast to evolution- traits that exist as exaptations in nondesert ary adaptations, exaptations are traits that species will determine how well they can evolved in response to specific past selection cope with droughts, and comparing their pressures, and provide a fitness advantage in degree of flexibility with those of species the prevailing environment under different from semideserts will enable us to predict selection pressures, meaning that the past their resilience. and current environments are different for at least some specific aspects (Gould and Lewontin 1979). In other words, these traits Evolutionary Adaptation, provide a function in their current role, but Adaptive Phenotypic Plasticity, were not selected for this purpose (Gould and Exaptations and Vrba 1982). For example, Hoffman Evolutionary adaptation involves genetic (2014) proposed that euryhalinity (i.e., sa- changes over generations (Rezende and linity tolerance) in the green toad Bufo vir- Diniz-Filho 2012). Over time, species may idis evolved to facilitate migration across the show genetic changes, leading to changes in variable habitats of Eurasia and the North morphology (e.g., peppered moths Biston African Mediterranean coastal regions. These betularia; Saccheri et al. 2008), physiology toads now occupy arid and semiarid regions,

This content downloaded from 137.219.126.019 on May 31, 2016 18:08:34 PM All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c). June 2016 Species Resilience to Droughts 139 suggesting that euryhalinity is an exaptation can be divided into developmental plasticity important for drought resistance (Hoffman and phenotypic flexibility (Piersma and van 2014). Euryhalinity in these toads did not Gils 2010; Box 1). For developmental plas- evolve in response to direct selection pres- ticity (Nettle and Bateson 2015), the envi- sure from an arid or semienvironment (i.e., ronment during early ontogeny determines evolved in response to past selection pres- which one of two or more developmental sure), but it does have current utility (i.e., pathways is adopted, leading to alternative provides a use in the existing context). The adult phenotypes that cannot change to any usefulness of the term exaptation has fre- of the other phenotypes (Ledón-Rettig et al. quently been criticized because exemplary 2008). The resulting phenotype is often ro- traits are often not clearly distinguishable bust, being able to cope with environmental from adaptations (Larson et al. 2013). The changes. For developmental plasticity to be distinction between adaptation and exap- adaptive, the population must have experi- tation is particularly important to consider enced particular environments in the past when assessing whether an individual could and, as a result, the developmental input to survive in a future environment not expe- produce particular phenotypes under par- rienced previously, as is predicted under ticular sets of conditions experiences posi- accelerated environmental change (Sih et tive selection (Nettle and Bateson 2015). In al. 2011). Existing phenotypic plasticity is other words, individuals experience a partic- likely to be of importance in the prevailing ular environment during early development environment, even if it has evolved under that is predictive of the environmental con- different selection pressures in a different ditions they are likely to experience in later environment (i.e., exaptive phenotypic plas- life. In the case of phenotypic flexibility, the ticity; Box 1). Therefore, a population might trait can change back and forth (i.e., it is re- be able to respond to increased severity of versible), such as changes of the osmoregu- droughts, not because it previously experi- latory hormone arginine vasopressin (AVP), enced droughts and is adapted to droughts, whose levels increase when the organism but because it experienced different envi- has to save water, but later decrease again. ronmental conditions that imposed similar Importantly, individuals may have both de- selection pressures (e.g., food shortage). velopmentally plastic traits and also pheno- This population could thus possess benefi- typically flexible traits. cial exaptations in response to droughts. One specific case of developmental plas- Adaptive phenotypic plasticity is an evolved ticity is epigenetic variation (Piersma and trait, enabling a comparatively rapid response van Gils 2010; Champagne 2013). Epige by individuals to cope with environmental netic mechanisms can also be influenced change. Phenotypic traits are altered adap- by hormones, which can link organizational tively in response to prevailing environmen- effects of hormones to differences in behav- tal conditions, which increases individual ior (Champagne and Rissman 2011). Impor- fitness (Charmantier et al. 2008; Ozgul et tantly, epigenetic inheritance can occur via al. 2009, 2010; Piersma and van Gils 2010). at least four different pathways, including Adaptive phenotypic plasticity may deter- cellular epigenetic inheritance (information mine an individual’s survival and reproduc- transmitted via the gametes), developmen- tion in the short term, which may facilitate tal inheritance (information transmitted via population persistence and evolutionary maternal effects), behavioral inheritance (in adaptation in the long term (West-Eberhard formation transmitted via niche construc- 1989; Hoffmann and Sgrò 2011). This could tion), and symbiotic inheritance ( Jablonka be especially important for juveniles and and Lamb 2005, 2007; Piersma and van Gils subadults that might be more vulnerable to 2010). Several recent reviews have focused stressful conditions than adults (e.g., Rivers on the links between epigenetics and pheno- et al. 2012). Importantly, adaptive phenotypic plasticity (e.g., Reik 2007; Champagne typic plasticity itself is the product of evolu- and Rissman 2011; Champagne 2013; Bale tion (Baldwin 1896). Phenotypic plasticity 2015; Dochtermann et al. 2015). However,

This content downloaded from 137.219.126.019 on May 31, 2016 18:08:34 PM All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c). 140 THE QUARTERLY REVIEW OF BIOLOGY Volume 91 the majority of studies on phenotypic plas- species from nondesert environments when ticity provide little or no information on the exposed to droughts, as an exaptation that underlying genetic and epigenetic mecha- evolved to save water under different envi- nisms. Therefore, in the context of this re- ronmental conditions, such as during win- view, we consider plasticity in general, rather ter or during periods when food has a lower than in relation to the absolute underlying water content due to seasonal changes. In mechanisms, by determining how variable sum, phenotypic plasticity can have very low the trait can be under varying environmen- flexibility (being fixed) or high flexibility, tal conditions. and represent adaptations or exaptations to Phenotypic plasticity has been hypothe- droughts. sized to be costly because of the need for the development and continued maintenance of neural structures (Dukas 1999), Three Primary Stressors and sensory and/or response pathways in- of Arid Environments volved in facilitating the flexible response Identifying the limits of phenotypic plas- (DeWitt et al. 1998; Mery and Burns 2010). ticity is foundational for assessing the degree However, estimating the actual costs of to which individuals can respond to rapid plasticity is difficult, and these costs might environmental change. To evaluate which be more easily detected under certain con- adaptations and exaptations could promote ditions. For example, costs of plasticity are species persistence to increased periodicity said to be greater in stressful conditions, and/or intensity of droughts, we will fo- and if plasticity utilizes resources that be- cus on species that currently inhabit areas come scarce in response to the stress, these characterized by periods of dryness (i.e., costs would be easier to detect (Steiner and semideserts and deserts) with low annual Van Buskirk 2008). Van Buskirk and Steiner precipitation and high aridity index (Box 1). (2009) argue that the costs of plasticity are Deserts and semideserts are characterized actually relatively weak and there might by three principal environmental stressors, be a compromise or tradeoff between the namely low water availability, low food avail- fitness benefits and costs of greater phe- ability, and extremes in temperature. The notypic plasticity. One of the main costs definition of “drought” is a relative one, taken of plasticity might be the time needed to to mean that current precipitation falls signifi- mount an appropriate plastic response. Be- cantly below the long-term mean of a defined cause plasticity seems to have surprisingly area (Dai 2011). In this context, drought is low costs, it has been argued recently that defined on a temporal scale and can occur in relaxed and variable selection intensities any environment. In contrast, naturally dry are more important constraints for the evo- areas, such as deserts, experience permanent lution of plasticity than are its costs (Mur- water shortage, and semideserts experience ren et al. 2015). seasons with water shortage. An aridity in- Phenotypic plasticity, enabling a coping dex, used in conjunction with total rainfall, response to droughts, can either be evolu- enables us to categorize habitats based on tionary adaptations (adaptive phenotypic water availability (e.g., deserts versus semi- plasticity) or exaptations (exaptive pheno- deserts; Nash and Engineering Group Work- typic plasticity). For example, all mammals ing Party 2012). Hyperarid areas, such as the have the hormone AVP, which is important northeastern parts of the Negev Desert in Is- in osmoregulation, but not all mammals rael (Boroda et al. 2014), experience more have experienced droughts as a selection than 12 months without rainfall, have less pressure modifying the AVP system. There- than 25mm rainfall/annum, and an average fore, an increase of AVP plasma levels to aridity index below 0.05, whereas arid areas, reduce water loss during droughts might such as the Namib Desert in southwestern be higher in desert species, representing an ad- Africa (Viles and Goudie 2013), receive less aptation to previous droughts, but would also than 100mm of rainfall per year, which is of- occur—although maybe at a lower level—in ten very unreliable, and have an aridity index

Working Party 2012). In our review, we group fluctuations in Ta that can range from very both arid categories into “deserts,” as the se- cold at night to very hot during the day, a lection pressures in both habitat types will consequence of reduced absorption of heat drive the establishment of specialized adap- by vegetation (Sarma et al. 2001), leading tations (see below). Semideserts, such as the to greater reflection of solar radiation by Hardeveld of the Succulent Karoo in South the ground during the day (i.e., increased Africa (Acocks 1988) and the Victoria River albedo; Charney et al. 1977), and rapid loss district in Australia (Webb et al. 2014), gen- of heat at night (Sarma et al. 2001). Animals erally receive between 100 and 200mm of living in naturally dry environments have rainfall per year on average, have a moderate evolved under selective pressures of fluctu- aridity index of between 0.2 and 0.5, and a ating temperature and tend to show specific 25–50% interannual rainfall variability (for behavioral, physiological, and/or morpho- definition see Box 1; Nash and Engineer- logical adaptations to these environmental ing Group Working Party 2012). We define extremes. For example, several large des- “drought-affected areas” as those that are nei- ert artiodactyls (Table 1), such as camels ther deserts nor semideserts, but experience Camelus dromedarius (Elkhawad 1992; Ouajd unpredictable droughts, which might occur and Kamel 2009) and Arabian oryx Oryx leu- more often and become more intense in the coryx (Hetem et al. 2012), utilize the carotid future due to climate change (Box 1). rete, a network of interlacing arterioles in Deserts and semideserts are characterized the venous sinus, for selective brain cooling by low food availability. Under these condi- (Hetem et al. 2012). Venous blood cooled tions, vegetation is typically sparse and patch- through the nasal countercurrent exchange ily distributed across the landscape (Zhang mechanism (Ouajd and Kamel 2009) drains et al. 2005). Consequently, food availability into the venous sinus, cooling the arterial and quality is spatially and temporally vari- blood moving to the brain (Mitchell et al. able and the availability of food resources 1987). might be unpredictable. For example, some To identify flexible traits that could con- areas might experience seasonal periods fer a fitness advantage under conditions of dryness, which are relatively predictable of increasing aridity, it is useful to study (predictable environment; Box 1), while species that inhabit deserts or semideserts. other areas might experience unpredictable, Categorizing species living in these dry extreme climatic events leading to droughts environments can help us to: identify key (unpredictable environment; Box 1). Ani- adaptations that have arisen in response mals inhabiting these environments have to to aridity; establish a comparative database cope both with periods of low water availabil- of traits that can be used to compare with ity and simultaneously low food availability other species for which we lack information; (Willmer et al. 2000). One important con- and recognize traits in nondesert-adapted sideration is that plants in deserts are also species that could promote responses to in- adapted to low water availability (Chaves et creasing aridity and droughts. al. 2003), whereas plants in areas experienc- ing increased frequencies of droughts due to climate change may not be adapted to cope Categorizing Species From with dry conditions over long periods (Vi- Deserts and Semideserts as cente-Serrano et al. 2013). As a result, food Endurers or Evaders and water availability in drought-affected ar- Willmer et al. (2000) classified desert an- eas may have an even greater influence on imals into two main groups—physiological animal populations than those in naturally endurers, such as the Arabian oryx, which dry areas. are able to tolerate environmental ex-

Ambient temperature (Ta) is the third fac- tremes using physiological and morpholog- tor inﬂuencing species in naturally dry and ical adaptations (Table 1) and behavioral in drought-affected areas. These habitats evaders, such as Merriam’s kangaroo rat

Table 1 Characteristic desert adaptations of physiological endurers and behavioral evaders Principal examples Behavior Physiology Morphology and references Mechanisms for coping with water restriction Physiological endurers 1 Camel Camelus dromedarius • Can go for extended • Constant [1a,b, but see 1o] or decreased [1f,s] • Nasal countercurrent a Schmidt-Nielsen et al. 1956 periods without plasma volume exchange system [1j,s], b Macfarlane et al. 1963 drinking [1l,o], [2b,e,f ], shows • Increased plasma Na [1b,d,f,i,o,s], protein [4d,j] c Schmidt-Nielsen et al. 1967 water independence [4c], [1f,s], [2e], sugar [1s], cholesterol [1s], and • Well-developed nasal d Siebert and Macfarlane 1971 or may survive on water urea [2g, but see 1g,k] concentration glands [1s] e Maloiy 1972 gained through food • Increased plasma arginine • Nostrils can close f Siebert and Macfarlane 1975 [2d,e,f,g,h], [3f,k], [4j] vasopressin [1o], [3b,k], aldosterone [1i], completely [1s] g Emmanuel et al. 1976 • Reduced food intake [1o] and renin [1i,o] secretion • Kidney with long loops h Young 1976 • Decreased insulin secretion [3k] of Henle and well- i Finberg et al. 1978 • Maintenance [2g] or increased plasma developed medulla [1s] j Schmidt-Nielsen et al. 1981a osmolality [2e], [3k] • Increased tubular k Yagil 1985 • Increased urine concentration [1o,s], reabsorption of the l Gihad et al. 1989 [2g], [3a,c,j,k], [4a,e,j] kidney [1s], [2g] m Wilson 1989 • Reduced urine production [1f,o,s] and • Thin erythrocyte with n Elkhawad 1992 volume [1a,b,i], [2g], [3k] increased surface area: o Ben Goumi et al. 1993 • Low glomerular filtration rate [1f,s] volume ratio [1s] p Faye 1997 • Increased urine Na excretion [1o] q Selim et al. 1999 • High tolerance to salt [1e], [3k] r Dereje and Udén 2005 • Excretion of relatively dry feces [1a,b,f,i], s [2g], [4b,j] Ouajd and Kamel 2009 2 Arabian oryx Oryx leucoryx • Reduction in metabolic rate [1c], [2d,h], a Hetem et al. 2010 [3a,c,d,e,f,g,j,m], [4j] b Stewart 1963 • Reduction in evaporative water loss c [1a,b,i], [2d,g], [4c,j] Spalton 1999 d Williams et al. 2001 • Production of metabolic water [2d], [4c] e Ostrowski et al. 2002 • Low water turnover [1a,b,i] f Ostrowski et al. 2003 • Increased urine creatinine g Ostrowski et al. 2006 concentration [2g] and decreased h Gilad et al. 2008 creatinine clearance [1s] Behavioral evaders • Decreased respiration rate [1c,k,m,s], [2g] 3 Golden spiny mouse Acomys • Reduction of digestive secretions [1s] russatus Mechanisms for coping with food restriction a Shkolnik and Borut 1969 b Castel and Abraham 1972 • Specialist feeder [1r,s], [4i] • Maintenance [3f,m] or minimal loss of • Reduction in organ c Haim and Borut 1981 or favors specific food body mass [1a,f,s], [2g] for physiological size/volume [2g] d Rubal et al. 1992 type [2c,d], [3i] endurers, but tolerance to loss of • Strong digestive e Haim and Izhaki 1993 • Feeds on water-rich body mass [3j,k] for behavioral evaders efficiency [1q,s], [2g] f Kam and Degen 1993 invertebrates [3i] or green • Mobilization of hepatic lipids [1s] and • Storage of fat/lipids g Merkt and Taylor 1994 matter [1s], [2g], or digs up fatty acids [2g] to fuel metabolism [1r], [3m] h Haim and Rozenfeld 1995 water-rich underground • Decreased leptin production [2g], [3m] i Mendelssohn and Yom-Tov plant storage organs [2c] • Good aptitude for recycling nitrogen 1999 • Stores/caches food [2b] [1g] j Ron and Haim 2001 • Exploits newly emergent • Enters torpor [3l,m] k Shanas and Haim 2004 food material [2g] l Ehrhardt et al. 2005 • Migratory behavior [1f,l,s), m Gutman et al. 2006 [2b] or shifting home range to areas with ephemeral high food abundance [2h], [4h]

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Table 1 Continued Principal examples Behavior Physiology Morphology and references Mechanisms for coping with extreme temperatures 4 Merriam’s kangaroo rat Dipodomys merriami • Utilizes burrows/nests • Adaptive heterothermy [1o], [2a,f] • Subdivision of nasal a Schmidt-Nielsen et al. [4f,j], cover [3h], or retreats • Adaptive hyperthermia [1c] sinus [1j], [4d,g] 1948 to shade when available • Storage of body heat during the day • Limited subcutaneous b Schmidt-Nielsen and [1s], [2d,g] and dissipation at night [1c] fat deposition [1h,s] Schmidt-Nielsen 1951 • Utilizes substrate • Higher stable hematocrit [1p], [2e] • Short coarse pelage [2b] c Schmidt-Nielsen and surface for conductance • Increased erythrocyte circulation • Light-colored pelage Schmidt-Nielsen 1952 of body heat [2b,d] efficiency [1s], erythrocyte volume for reflecting solar d Jackson and Schmidt- • Primary activity: flexibility [1s], and enhanced radiation and reducing Nielsen 1964 crepuscular or erythrocyte life span [1s] heat uptake [2b] e Carpenter 1966 nocturnal [2b,d,g] • Low cardiac rate and low blood • Maintenance of f Soholt 1974 • Decreased activity [2g] pressure [1s] nonshivering g Schmidt-Nielsen et al. 1970 • Bipedal locomotion [2b] • Selective brain cooling [1n,s] thermogenesis [3e] h Brown and Munger 1985 • Minimizes exposure to • Enters torpor [3l,m] • Dark pigmented i Mares 1993 sun by altering body skin [3h] j Nagy 1994 posture [1p,s] • Does not pant [1c,s]

Superscript numbers designate species (endurers: 1Camelus dromedarius, 2Oryx leucoryx; evaders: 3Acomys russatus, 4Dipodomys merriami) and letters designate associated references, which appear in Appendix 1.

Dipodomys merriami, which are able to es- of exaptive phenotypic plasticity, which we cape environmental extremes behaviorally consider to be a key mechanism to cope (Table 1). Later, Ward (2009) recognized with change, including droughts. As such, that endurers are typically large-bodied the endurer-evader categorization provides animals while evaders are typically small- an initial framework from which to further bodied animals. identify important traits to be studied in The endurer-evader concept is useful for nondesert-adapted species for coping with categorizing desert specialists primarily in heat, food, and water restriction as a conse- relation to one characteristic of arid envi- quence of droughts. ronments, namely extremes in environmental temperature (Ta). However, this concept is a simplistic approach, based on the as- A Novel Classification: The sumption that it is easier for small animals Adaptive Triquetra to find refuge in the shade than it is for Given the simplicity of the endurer-evader large animals, while in fact we know that concept, we developed a three-tier system, large animals will use any little shade they the adaptive triquetra, that categorizes ad- can find in their environment to avoid high aptations to aridity instead of categorizing

Ta (Williams et al. 2001; Ostrowski et al. species (Box 2). Having a species catego- 2006; Ouajd and Kamel 2009). Although rization is not helpful for generalizing ad- this concept, to a degree, considers the aptations across species, and importantly ability of animals to be behaviorally flexi- overlooks the underlying general adaptive ble (e.g., seeking shade), it generally as- responses to drought. We stress that provid- sumes that animals have limited flexibility ing this framework is only the first step. The in their behavioral and morphological re- framework we develop here must be vali- sponses and neglects the important aspect dated in the future by data from a variety

Box 2 Using the adaptive triquetra system The adaptive triquetra considers a three-step approach that can be used for either: directly assessing resilience in species for which good biological information al- ready exists; and/or for identifying areas where more research may be required. For example, if someone is interested in a particular species, they might have good knowledge of its life history, but little knowledge about its environment, and could therefore focus on establishing which environmental stressor is more important before understanding how the species could respond. Similarly, someone might have good knowledge about the physiology of a species, but little about its behavior. Focus could be placed on how that species responds behaviorally to particular environmental stressors.

Step 1 Step 2 Step 3 What is the primary What traits correspond What is the relative environmental stressor? to each body system? flexibility of each trait?

Step 1: What is the Primary Environmental Stressor? ( Water, Food, Temperature) Consider the environment in which the species of interest occurs, and what the primary stressor would be, taking microhabitat use into account (Tables 2a, b, and c). This is important because not all habitats will experience the same intensity of change and some environments will buffer some stressors better than others. For example, temperature extremes might be more critical in subtropical areas experi- encing droughts than in temperate or polar climate zones. For a diurnal burrowing rodent, such as Brants’s whistling rat Parotomys brantsii ( Jackson et al. 2004), extreme temperatures may not represent a problem due to the buffering effects of burrows. Step 2: What Traits Correspond to Each Body System? (Behavioral, Physiological, Morphological) This step considers the presence of, and number of traits, corresponding to each system (Tables 2a, b, and c). The greater the number of traits allowing for coping with the stressors, the more likely it is that the species might be able to cope with rapid environmental changes. However, this will also heavily depend on the flexibility of the traits (Step 3). Step 3: What is the Relative Flexibility of Each Trait? (Fixed, Developmentally Plastic, Flexible) The ability of a species to persist under increasing likelihood of droughts is dependent on how individuals are able to respond with the traits they possess. An individual has a greater likelihood of responding to unpredictable events if it has greater flexibility (Tables 2a, b, and c). The interaction between two traits can also change the potential for resilience. For example, the interaction between a fixed morphological trait and a flexible behavioral trait is important for African striped mice Rhabdomys pumilio in the Succulent Karoo of South Africa. Striped mice have dark skin (Schradin and Pillay 2005), which facilitates thermoregulation through basking (Schradin et al. 2007), allowing mice to conserve energy in the early morn- ing when temperatures are lower.

This content downloaded from 137.219.126.019 on May 31, 2016 18:08:34 PM All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c). June 2016 Species Resilience to Droughts 145 of different species and different research survival. Therefore, supplemental feeding in programs to determine its accuracy, and Klaserie could have been highly beneficial to then modified as appropriate. Our compre- promote species survival. hensive review of adaptations to droughts of specialist and nonspecialist species provides the foundational information needed which stressor is addressed? for such future research programs on the The first step of the adaptive triquetra effects of droughts on individual survival model is to identify which of the three pri- and population and species persistence. mary stressors has driven the evolution of The term “triquetra” is derived from the the particular adaptation in question (Box 2). Latin tri- “three” and quetrus “cornered,” First, low water availability leads to the need emphasizing the three-tiered nature of this for improved osmoregulation, resulting in classification system, as well as the intercon- adaptations that reduce water loss or in- nectedness of its parts. Our adaptive triquetra crease water intake (Table 2a). Second, since considers: which stressor is addressed (water food availability is a direct consequence of restriction, food restriction, or extremes in water restriction, there is a need for im-

Ta); which body system mounts an appropri- proved energy storage mechanisms, result- ate adaptive response (behavior, physiology, ing in adaptations that minimize energy or morphology); and the nature of the trait loss or maximize energy gain (Table 2b). (fixed versus flexible). Although these stress- These include both intrinsic adaptations, ors are often interlinked (e.g., plants are such as storage of body fat (e.g., Mongolian dependent on water and, therefore, food is gerbils Meriones unguiculatus; Zhang and likely to be restricted if water is restricted), Wang 2007), and extrinsic adaptations, such we argue that each stressor should first be as food caching (e.g., kangaroo rats Dipo examined independently, because some spe- domys spp.; Randall 1993). Third, high Ta cies might have adaptations or exaptations leads to the need for improved thermoreg- that facilitate better coping with one stressor ulatory ability, resulting in adaptations that compared to another. This is especially im- decrease the risk of overheating or increase portant for designing effective management the ability to tolerate heat (Table 2c). strategies to support populations at risk. For These three stressors are not fully inde- example, during a severe drought period pendent of each other. For example, in (1981–1984) in southern Africa, mortality of mammals, the need for improved thermo- herbivores was quite high, but in some areas, regulation is directly related to the need such as the northeastern Tuli region of Bo- to save water because the ability to reduce tswana, mixed grazers-browsers (e.g., impala water loss in mammals is constrained by Aepyceros melampus) were little affected com- the need for evaporative cooling to reduce pared to grazers (e.g., blue wildebeest Con- overheating (Taylor 1970). Furthermore, nochaetes taurinus and zebra Equus burchelli), water can be obtained from food directly whereas in other areas, such as the central (e.g., consumption of succulents by visca Kruger National Park in South Africa, the cha rats Octomys mimax; Bozinovic and Con- same grazers (blue wildebeest and zebra) treras 1990) and/or indirectly (e.g., use of were unaffected (Walker et al. 1987). Walker metabolic water by the desert pocket mouse et al. (1987) suggest that mortality in Kla- Chaetodipus penicillatus; Grubbs 1980). How- serie Reserve in South Africa (adjacent to ever, most animals cannot obtain sufficient the Kruger National Park) was heightened water from their food to survive without by close spacing of permanent water sources. access to freestanding water or condensed Heavy grazing occurred around these areas, water. For species that are dependent on eliminating reserve stands. Instead, drop- freestanding water, the primary stressor will ping fences and widely spacing water sources be water availability, whereas for water-in- would have allowed animals to move be- dependent species, the primary stressor tween areas, accessing forage and promoting will be food availability.

Table 2a The adaptive triquetra system for the environmental stressor water restriction

Nature of Selected Present in my Degree of plasticity System the trait Trait Example species references study species? or flexibility?

Behavior Flexible Consumes water-rich Semidesert food resources or • African striped mouse Schradin and Pillay green matter Rhabdomys pumilio 2005b • Black-tailed tree rat Frean et al. 1998 Thallomys nigricauda • Springbok Antidorcas Nagy 1994 marsupialis Desert • Arabian oryx Oryx leucoryx Stewart 1963 • Banner-tailed kangaroo Schmidt-Nielsen rat Dipodomys spectabilis and Schmidt- Nielsen 1952 Reduces food intake Semidesert • African striped mouse Schradin et al. 2010 Rhabdomys pumilio • Kirk’s dik-dik Madoqua Maloiy 1973 kirkii • Namaqua rock rat Buffenstein 1985 Aethomys namaquensis Desert • Camel Camelus Ben Goumi et al. dromedarius 1993 • Jackrabbit Lepus Reese and Haines californicus 1978 Alters home range Semidesert or changes • African buffalo Syncerus Funston et al. 1994 distribution to caffer increase access • Mehely’s horseshoe bat Salsamendi et al. to water/take Rhinolophus mehelyi 2012 advantage of new Desert water sources • Desert mule deer Rautenstrauch and Odocoileus hemionus crooki Krausman 1989 • Hairy-footed gerbil Christian 1980 Gerbillurus paeba Drinks sea water or Semidesert tolerates high salt • Mongolian gerbil Meriones Winkelmann and content in food unguiculatus Getz 1962 • Tammar wallaby Macropus Purohit 1971 eugenii Desert • Desert bighorn sheep Turner 1979 Ovis canadensis nelsoni • Fawn hopping mouse MacMillen and Lee Notomys cervinus 1969 Fixed Can go for extended Semidesert periods without • Eland Tragelaphus oryx King et al. 1975 drinking, but is • European free-tailed bat Rainho 2007 not independent Tadarida teniotis of water Desert • Camel Camelus Schmidt-Nielsen dromedarius et al. 1956 • Eastern Patagonian Mares 1977a laucha Eligmodontia typus Physiology Flexible Increases arginine Semidesert vasopressin • African striped mouse Schoepf and secretion and/or Rhabdomys pumilio Schradin 2014 replenishes AVP • Degu Octodon degus Bozinovic et al. 2003 store • Ethiopian Somali goat Mengistu et al. 2007 Capra aegagrus hircus

continued

Table 2a Continued

Nature of Selected Present in my Degree of plasticity System the trait Trait Example species references study species? or flexibility?

Desert • Camel Camelus dromedarius Ben Goumi et al. 1993 • Golden spiny mouse Castel and Abraham Acomys russatus 1972 Increased plasma Semidesert aldosterone • Awassi sheep Ovis aries Jaber et al. 2004 and/or renin • Common spiny mouse Bukovetzky et al. secretion, often Acomys cahirinus 2012 in response to Desert rehydration • Black Bedouin goat Capra Wittenberg et al. aegagrus hircus 1986 • Tarabul’s gerbil Gerbillus Saadi and Lebaili tarabuli 2012 Decreased thyroxine Semidesert secretion • Awassi sheep Ovis aries Jaber et al. 2011 • Cactus mouse Peromyscus Hulbert et al. 1985 eremicus Desert • Marwari sheep Ovis Kataria and Kataria aries 2006 • Merriam’s kangaroo rat Yousef and Johnson Dipodomys merriami 1975 Increased urine Semidesert concentration • African striped mouse Buffenstein 1984 Rhabdomys pumilio • Bush karoo rat Otomys Jackson et al. 2004 unisulcatus • Kirk’s dik-dik Madoqua Hoppe 1977 kirkii Desert • Arabian oryx Oryx leucoryx Ostrowski et al. 2006 • Merriam’s kangaroo rat Nagy 1994 Dipodomys merriami Reduced urine Semidesert production and • Bushy-tailed hairy-footed Downs and Perrin volume gerbil Gerbillus vallinus 1990 • Dorcas gazelle Gazella dorcas Ghobrial 1970 Desert • Arabian oryx Oryx leucoryx Ostrowski et al. 2006 • Spinifex hopping mouse MacMillen and Lee Notomys alexis 1969 Excretion of Semidesert relatively dry feces • Kirk’s dik-dik Madoqua kirkii Maloiy 1973 • Springhare Pedetes Peinke and Brown capensis 1999 Desert • Agile kangaroo rat Schmidt-Nielsen and Dipodomys agilis Schmidt-Nielsen 1952 • Desert bighorn sheep Turner 1970 Ovis canadensis nelsoni Decreased Semidesert respiration rate • Eland Tragelaphus oryx Taylor 1969 • Rock hyrax Procavia Rübsamen and capensis Kettembeil 1980 Desert • Arabian oryx Oryx leucoryx Ostrowski et al. 2006 • Spinifex hopping mouse Withers et al. 1979 Notomys alexis

continued

Table 2a Continued

Nature of Selected Present in my Degree of plasticity System the trait Trait Example species references study species? or flexibility?

Utilization of Semidesert metabolic water • Mongolian gerbil Meriones Winkelmann and to reduce overall unguiculatus Getz 1962 water loss • Siorhi goat Capra aegagrus Misra and Singh hircus 2002 Desert • Desert pocket mouse Grubbs 1980 Chaetodipus penicillatus • Rüppell’s fox Vulpes Williams et al. 2002 rueppelli Increased tubular Semidesert reabsorption of • Degu Octodon degus Bozinovic et al. 2003 water from the • Kirk’s dik-dik Madoqua kirkii Maloiy et al. 1988 kidney or the Desert bladder • Arabian oryx Oryx leucoryx Ostrowski et al. 2006 • Agile kangaroo rat Howell and Gersh Dipodomys agilis 1935 Maintenance or Semidesert higher hematocrit • Awassi sheep Ovis aries Laden et al. 1987 • Springhare Pedetes capensis Peinke and Brown 1999 Desert • Pronghorn Antilocapra McKean and Walker americana 1974 • Spinifex hopping mouse Heimeier and Notomys alexis Donald 2006 Mobilization of Semidesert hepatic lipids and • African striped mouse Fourie and Haim fatty acids to fuel Rhabdomys pumilio 1980 metabolism • Least gerbil Gerbillus Buffenstein 1984 * And/or in pusillus response to food • Awassi sheep Ovis aries Jaber et al. 2011 availability Desert • Arabian oryx Oryx leucoryx Ostrowski et al. 2006 • Hairy-footed gerbil Buffenstein 1985 Gerbillurus paeba Enters torpor (or Semidesert hibernation) • Grey mouse lemur Schmid and * And/or in response Microcebus murinus Speakman 2009 to temperature • Cactus mouse Peromyscus MacMillen 1965 extremes and eremicus food restriction. Desert Information on • Pinyon mouse Peromyscus Bradford 1974 this topic is limited truei and equivocal • Stripe-faced dunnart Song and Geiser (Geiser 2010) Sminthopsis macroura 1997 Information on large mammals is lacking in the literature Fixed Shows water Semidesert independence • Drylands vesper mouse Mares 1977b Calomys musculinus • Springbok Antidorcas Nagy and Knight marsupialis 1994 Desert • Desert leopard Panthera Bothma and Riche pardus 1984 • Peruvian desert mouse Koford 1968 Phyllotis gerbillus

continued

Table 2a Continued

Nature of Selected Present in my Degree of plasticity System the trait Trait Example species references study species? or flexibility?

Maintenance or Semidesert tolerance of • German mutton merino Degen 1977 decreased plasma sheep Ovis aries volume • Springhare Pedetes capensis Peinke and Brown 1999 Desert • Camel Camelus Siebert and dromedarius Macfarlane 1975 • White-tailed antelope Hartman and squirrel Ammospermophilus Morton 1973 leucurus Maintenance or Semidesert increased plasma • Degu Octodon degus Bozinovic et al. 2003 osmolality • Tammar wallaby Macropus Kinnear et al. 1968 (sodium, protein, eugenii sugar, cholesterol, Desert and/or urea) • Barmer goat Capra Khan et al. 1978 aegagrus hircus • Desert wood rat Neotoma MacMillen and Lee lepida 1967 Tolerates increased Semidesert urinary urea • Kirk’s dik-dik Madoqua Maloiy 1973 concentration kirkii • Namib brush-tailed gerbil Buffenstein et al. Gerbillurus setzeri 1985 Desert • Camel Camelus Emmanuel et al. dromedarius 1976 • Kowari Dasyuroides byrnei Haines et al. 1974 Production of Semidesert allantoin • Bushveld gerbil Gerbilliscus Buffenstein et al. precipitate in leucogaster 1985 place of urea • Cape gerbil Gerbilliscus Buffenstein et al. * Lack of evidence in afra 1985 larger mammals Desert • Dune hairy-footed gerbil Downs and Perrin Gerbillurus tytonis 1991 • Gerbil mouse Malacothrix Buffenstein et al. typica 1985 Low glomerular Semidesert ﬁltration rate • Kirk’s dik-dik Madoqua Rugangazi and kirkii Maloiy 1988 • Least gerbil Gerbillus Buffenstein 1984 pusillus Desert • Black Bedouin goat Capra Wittenberg et al. aegagrus hircus 1986 • Merriam’s kangaroo rat Schmidt-Nielsen and Dipodomys merriami Schmidt-Nielsen 1952 Reduced metabolic Semidesert rate • African striped mouse Haim and Fourie Rhabdomys pumilio 1980a • Damara ground squirrel Haim et al. 1986 Xerus princeps • Kirk’s dik-dik Madoqua kirkii Hoppe 1977 Desert • Euro Macropus robustus Dawson et al. 1975 erubescens • Viscacha rat Octomys Bozinovic and mimax Contreras 1990

continued

Table 2a Continued

Nature of Selected Present in my Degree of plasticity System the trait Trait Example species references study species? or flexibility?

Reduction in Semidesert evaporative water • African striped mouse Christian 1978 loss Rhabdomys pumilio • Kirk’s dik-dik Madoqua Maloiy 1973 kirkii • Panamint kangaroo rat Hinds and Dipodomys panamintinus MacMillen 1985 Desert • Desert kangaroo rat Hinds and Dipodomys deserti MacMillen 1985 • Gemsbok Oryx gazella Taylor 1969 Low water turnover Semidesert • African striped mouse Scantlebury et al. Rhabdomys pumilio 2006 • Shaw’s jird Meriones shawi de Roufﬁgnac and Morel 1965 • Tammar wallaby Macropus Kinnear et al. 1968 eugenii Desert • Namib desert golden mole Fielden et al. 1990 Eremitalpa granti namibensis • Red kangaroo Macropus Dawson et al. 1975 rufus Good aptitude for Semidesert recycling (urea) • Rock hyrax Procavia Hume et al. 1980 nitrogen capensis • Tammar wallaby Macropus Kennedy and Hume eugenii 1978 Desert • Black Bedouin goat Capra Silanikove et al. aegagrus hircus 1980 • Fat sand rat Psammomys Kaißling et al. 1975 obesus Tolerates some level Semidesert of dehydration • Desert sheep Ovis aries El-Hadi 1986 • Springhare Pedetes capensis Peinke and Brown 1999 Desert • Burro Equus asinus Yousef et al. 1970 • Peruvian desert mouse Koford 1968 Phyllotis gerbillus Morphology Flexible Storage of water in Semidesert the stomach/ • African elephant Leggett 2004 rumen/ Loxodonta africana pharyngeal pouch Desert * Lack of evidence in • Camel Camelus Elkhawad 1992 smaller mammals dromedarius Fixed Nasal countercurrent Semidesert exchange system • Kirk’s dik-dik Madoqua Kamau et al. 1984 * Also provides kirkii a beneﬁt • Little red kaluta Withers and Cooper against high Dasykaluta rosamondae 2009 temperatures Desert • Camel Camelus dromedarius Elkhawad 1992 • Greater bilby Macrotis Hulbert and Dawson lagotis 1974

continued

Table 2a Continued

Nature of Selected Present in my Degree of plasticity System the trait Trait Example species references study species? or flexibility?

Kidney with Semidesert well-developed • Salt flat mouse Salinomys Diaz and Ojeda medulla and long delicatus 1999 loops of Henle • Tammar wallaby Macropus Kinnear et al. 1968 eugenii Desert • Camel Camelus Ouajd and Kamel dromedarius 2009 • Darwin’s leaf-eared Vermeulen and Nel mouse Phyllotis darwini 1988 darwini Elongated renal Semidesert papilla • Black-tailed tree rat Frean et al. 1998 * Large desert Thallomys nigricauda mammals do • Salt flat mouse Salinomys Diaz and Ojeda not show this delicatus 1999 characteristic Desert (Mbassa 1988) • Egyptian gerbil Gerbillus Khalil and Tawfic gerbillus 1963 • Plains viscacha rat Diaz and Ojeda Tympanoctomys barrerae 1999

Systems providing an appropriate adaptive response (behavior, physiology, or morphology); flexibility of traits (flexible or fixed). Fixed traits also include traits that show developmental plasticity during ontogeny. Researchers should identify the relative plasticity of fixed traits in particular environments (i.e., the reaction norm). A list of traits that could confer a fitness advantage under increasing likelihood of droughts, in relation to the three parts of the triquetra. We have included examples of a large- and small-bodied semidesert and desert species for each trait. The final two columns can be used by researchers and nature conservationists to categorize their study species, to identify areas where information is lacking, and to reach conclusions about the relative status of their species. The selected references appear in Appendix 1.

Table 2b The adaptive triquetra system for the environmental stressor food restriction.

Nature of Selected Present in my Degree of plasticity System the trait Trait Example species references study species? or flexibility?

Behavior Flexible Stores/caches food/ Semidesert scatter hoards • Black-backed jackal Canis Nel 1984 mesomelas • Giant kangaroo rat Shaw 1934 Dipodomys ingens Desert • Desert kit fox Vulpes Cypher 2003 macrotis arsipus • Wagner’s gerbil Gerbillus Hatough-Bouran dasyurus dasyurus 1990 Exploits newly Semidesert emergent food • African striped mouse Schradin and Pillay material Rhabdomys pumilio 2006 • Vicuña Vicugna vicugna Donadio et al. 2012 Desert • Arabian oryx Oryx leucoryx Ostrowski et al. 2006 • Piute ground squirrel Rickart 1986 Spermophilus mollis

continued

Table 2B Continued

Nature of Selected Present in my Degree of plasticity System the trait Trait Example species references study species? or flexibility?

Migratory behavior Semidesert or shifting home • African buffalo Syncerus Funston et al. 1994 range (mobility) caffer to areas with • African striped mouse Schradin and Pillay higher food Rhabdomys pumilio 2006 abundance • Round-eared sengi Schubert et al. 2009 Macroscelides proboscideus Desert • Banner-tailed kangaroo Brown and Munger rat Dipodomys spectabilis 1985 • Desert mule deer Albert and Odocoileus hemionus crooki Krausman 1993 Coprophagy Semidesert • Feral horse Equus caballus Krysl et al. 1984 • Southern mountain cavy Sassi et al. 2010 Microcavia australis Desert • African elephant Leggett 2004 Loxodonta africana • Noki Petromus typicus Rathbun and Rathbun 2005 Generalist feeder Semidesert • African striped mouse Curtis and Perrin Rhabdomys pumilio 1979 • Ash-grey mouse Pseudomys Murray et al. 1999 albocinereus • Tammar wallaby Macropus Kinnear et al. 1968 eugenii Desert • Camel Camelus dromedarius Dereje and Udén 2005 • Grey leaf-eared mouse Giannoni et al. 2001 Graomys griseoﬂavus Dietary ﬂexibility Semidesert • Drylands vesper mouse Giannoni et al. 2005 Calomys musculinus • Springbok Antidorcas Nagy and Knight marsupialis 1994 Desert • Brush-tailed mulgara Chen et al. 1998 Dasycercus blythi • Sand gazelle Gazella Schulz et al. 2013 marica Fixed Specialist feeder Semidesert • Black-tailed tree rat Frean et al. 1998 Thallomys nigricauda • Springbok Antidorcas Nagy 1994 marsupialis Desert • Arabian oryx Oryx leucoryx Spalton 1999 • Fat sand rat Psammomys Daly and Daly 1973 obesus Physiology Flexible Mobilization of Semidesert hepatic lipids and • African striped mouse Fourie and Haim fatty acids to fuel Rhabdomys pumilio 1980 metabolism • Least gerbil Gerbillus Buffenstein 1984 * And/or in pusillus response to water • Awassi sheep Ovis aries Jaber et al. 2011 availability Desert • Arabian oryx Oryx leucoryx Ostrowski et al. 2006 • Hairy-footed gerbil Buffenstein 1985 Gerbillurus paeba

continued

Table 2B Continued

Nature of Selected Present in my Degree of plasticity System the trait Trait Example species references study species? or flexibility?

Enters torpor (or Semidesert hibernation) • Grey mouse lemur Schmid 2001; Schmid * And/or in Microcebus murinus and Speakman 2009 response to water • North African elephant Lovegrove et al. restriction and shrew Elephantulus rozeti 2001 temperature Desert extremes. • Round-tailed ground Hudson 1964 Information on squirrel Spermophilus large mammals tereticaudus is lacking in the • Stripe-faced dunnart Song and Geiser literature Sminthopsis macroura 1997 Reduced leptin Semidesert secretion in • Awassi sheep Ovis aries Jaber et al. 2011 response to • Common spiny mouse Bukovetzky et al. starvation, Acomys cahirinus 2012 to reduce • Desert mobilization of • Arabian oryx Oryx leucoryx Ostrowski et al. 2006 fatty acid reserves • Golden spiny mouse Gutman et al. 2008 Acomys russatus Ecological leptin Semidesert hypothesis • African striped mouse Schradin et al. 2014 * This dissociation Rhabdomys pumilio between leptin • Mongolian gerbil Meriones Zhang and Wang and fattening is unguiculatus 2007 lacking in the • Desert literature • Golden spiny mouse Gutman et al. 2006 Acomys russatus Fixed Maintenance, Semidesert tolerance, or • Least gerbil Gerbillus Buffenstein 1984 minimal loss of pusillus body mass • Springbok Antidorcas Nagy 1994 marsupialis Desert • Camel Camelus Siebert and dromedarius, Macfarlane 1975 • Sandy inland MacMillen and Lee mouse Pseudomys 1967 hermannsburgensis Morphology Flexible Flexibility in length/ Semidesert mass of portions • Burro Equus asinus Sneddon et al. 2006 of the gut/ • Southern mountain cavy Sassi et al. 2007 intestine/and Microcavia australis mass of other vital Desert organs (e.g., liver, • Arabian oryx Oryx leucoryx Ostrowski et al. 2006 kidneys, cecum) • Darwin’s leaf-eared Naya et al. 2005 mouse Phyllotis darwini rupestris Storage of fat/lipids Semidesert (i.e., fattening) • African striped mouse Schradin and Pillay Rhabdomys pumilio 2005a • Awassi sheep Ovis aries, Khachadurian et al. 1966 • Fat-tailed dunnart Morton 1978 Sminthopsis crassicaudata Desert • Camel Camelus Elkhawad 1992 dromedarius • Golden spiny mouse Gutman et al. 2006 Acomys russatus

continued

Table 2B Continued

Nature of Selected Present in my Degree of plasticity System the trait Trait Example species references study species? or flexibility?

Fixed Strong digestive Semidesert efﬁciency • Degu Octodon degus Veloso and Bozinovic 1993 • Kirk’s dik-dik Madoqua kirkii Hoppe 1977 Desert • Arabian oryx Oryx leucoryx Ostrowski et al. 2006 • Great Basin pocket Schreiber 1979 mouse Perognathus parvus

which body system mounts an lethal diurnal temperatures, as well as mini- appropriate adaptive response? mizing water loss (Tables 2a and c). The second step of the adaptive triquetra Second, physiological traits of osmoregu- model is to identify which body systems lation, metabolism, and thermoregulation have changed in response to the environ enable individuals to offset the limited re- mental challenges associated with increasing sources of water and food, and to respond droughts (Box 2). We expect that all species to thermal stress (Tables 2a, b, and c). We may use multiple adaptive strategies at the need to differentiate between physiologi- behavioral, physiological, and morphological mechanisms of the three processes and cal levels to adapt to, and cope with, the pre- the physiological markers indicating devi- vailing environment. First, animals may use ation from the optimal physiological state, speciﬁc behaviors to avoid harsh environ- which could suggest that the individual is mental conditions. Animals can reduce wa- struggling to maintain homeostasis. For ter stress by choosing to consume water-rich example, decreased thyroxine levels could food, by reducing their food intake (thereby indicate a mechanism to save metabolic minimizing water required for digestion), energy (Yousef and Johnson 1975), while and/or by reducing respiration to mini- reduced blood glucose levels might not be mize evaporative water loss (Table 2a). An- an adaptation, but rather a physiological imals can reduce food stress by consuming marker of deviation (stress) from the opti- newly emergent food (e.g., plant/insect), mal physiological state (McCue 2010). by altering the diet to include a wider vari- Recently, the term allostasis has been used ety of food types (opportunistic feeders), or to describe the physiological mechanisms by storing or caching food (Table 2b). To that maintain stability (homeostasis of blood avoid temperature extremes, animals can glucose, pH, and O2 levels) through change employ a range of behavioral strategies to of the osmoregulatory, metabolic, and/or minimize overheating, such as utilizing bur- thermoregulatory system (McEwen and Wing rows/cover/shade that buffer temperature ﬁeld 2003). Importantly, allostasis depends extremes and also minimize water loss, or on the energy availability in the environment, altering body posture to minimize exposure which decreases during droughts, leading to to the sun (Tables 2a, b, and c). Altering ac- allostasis overload type 1 (energy expendi- tivity levels by shifting to nocturnal activity ture to cope with environmental stressors is another strategy minimizing exposure to is greater than energy intake; McEwen and

Table 2c

The adaptive triquetra system for the environmental stressor extremes in environmental temperature (Ta) Nature of Selected Present in my Degree of plasticity System the trait Trait Example species references study species? or flexibility?

Behavior Flexible Utilizes burrows/ Semidesert nests, cover, or • African striped mouse Schradin 2005 retreats to shade Rhabdomys pumilio when available • Giant kangaroo rat Randall 1997 Dipodomys ingens • Southern hairy-nosed Walker et al. 2007 wombat Lasiorhinus latifrons Desert • Euro Macropus robustus Dawson and Brown erubescens 1970 • Sundevall’s jird Meriones Lewis et al. 1965 crassus crassus Utilizes substrate Semidesert surface for • African striped mouse Schradin 2006 conductance of Rhabdomys pumilio body heat • Cape ground squirrel Marsh et al. 1978 * Information is Xerus inauris lacking for large • Suricate Suricata suricatta Hinton and Dunn semidesert species 1967 Desert • Desert mule deer Cain et al. 2006 Odocoileus hemionus crooki • White-tailed antelope Chappell and squirrel Ammospermophilus Bartholomew leucurus, 1981a Uses body parts to Semidesert facilitate shading • Cape ground squirrel Bennett et al. 1984 Xerus inauris • Springbok Antidorcas Fuller et al. 2005 marsupialis Desert • Camel Camelus Ouajd and Kamel dromedarius 2009 • White-tailed antelope Chappell and squirrel Ammospermophilus Bartholomew leucurus 1981b Activity variable or Semidesert polyphasic • Mongolian gerbil Meriones Lewis et al. 1965 unguiculatus • Black wildebeest Maloney et al. 2005 Connochaetes gnou Desert • Arabian oryx Oryx leucoryx Stewart 1963 • Lybian jird Meriones Aulagnier et al. 2008 libycus Primary activity— Semidesert crepuscular • African wild dog Lycaon Woodroffe 2011 pictus • Bush karoo rat Otomys Vermeulen and Nel unisulcatus 1988 Desert • King jird Meriones rex Alagaili et al. 2013 • Red kangaroo Macropus Dawson et al. 1975 rufus

continued

Table 2C Continued

Nature of Selected Present in my Degree of plasticity System the trait Trait Example species references study species? or flexibility?

Decreased activity Semidesert • African striped mouse Schumann et al. Rhabdomys pumilio 2005 • Degu Octodon degus Lagos et al. 1995 • Feral pig Sus scrofa Dexter 2003 Desert • Arabian oryx Oryx leucoryx Ostrowski et al. 2006 • Greater bilby Macrotis Hulbert and Dawson lagotis 1974 Social huddling at Semidesert night to minimize • African striped mouse Scantlebury et al. heat loss Rhabdomys pumilio 2006 • Brants’s whistling rat du Plessis et al. 1992 Parotomys brantsii • Vervet monkey Chlorocebus Lubbe 2013 pygerythrus Desert • Collared peccary Pecari Zervanos and tajacu Hadley 1973 • Spinifex hopping mouse Withers et al. 1979 Notomys alexis

Bask to increase solar Semidesert absorption • African striped mouse Schradin et al. 2007 Rhabdomys pumilio • Eland Tragelaphus oryx Hetem et al. 2011 • Fat-tailed dunnart Warneke et al. 2008 Sminthopsis crassicaudata Desert • Collared peccary Pecari Zervanos and tajacu Hadley 1973 • Fat-tailed antechinus Geiser and Pavey Pseudantechinus 2007 macdonnellensis Social ﬂexibility or Semidesert group ﬂexibility • African striped mouse Schradin et al. 2012 Rhabdomys pumilio • Hamadryas baboon Papio Schreier and hamadryas hamadryas Swedell 2012 • Round-eared sengi Schubert et al. 2009 Macroscelides proboscideus Desert • Great gerbil Rhombomys Randall et al. 2005 opimus • Pronghorn Antilocapra Deblinger and americana Alldredge 1989 Fixed Primary Semidesert activity—nocturnal • Greater Egyptian jerboa El Ouezzani et al. Jaculus orientalis 2001 • Tammar wallaby Macropus Kinnear et al. 1968 eugenii Desert • Desert bighorn sheep Hansen 1982 Ovis canadensis nelsoni • Yellow-rumped leaf- Tirado et al. 2008 eared mouse Phyllotis xanthopygus rupestris

continued

Table 2C Continued

Nature of Selected Present in my Degree of plasticity System the trait Trait Example species references study species? or flexibility?

Primary Semidesert activity—diurnal • African striped mouse Haim and Fairall Rhabdomys pumilio 1986 • Black wildebeest Mitchell et al. 2002 Connochaetes gnou • Brants’s whistling rat Jackson et al. 2004 Parotomys brantsii Desert • Fat sand rat Psammomys Ilan and Yom-Tov obesus 1990 • Nubian ibex Capra Hochman and nubiana Kotler 2006 Does not pant except Semidesert in the final stages • African buffalo Syncerus Taylor 1970a of heat stress caffer * Reflects a reflex to • Lesser long-nosed bat Carpenter and thermal extremes Leptonycteris yerbabuenae Graham 1967 (i.e., may not Desert have adaptive • Camel Camelus Ouajd and Kamel significance dromedarius 2009 for all species; • Greater bilby Macrotis Hulbert and Dawson Woodroffe 2011) lagotis 1974 Physiology Flexible Pants to reduce Semidesert temperature • Kirk’s dik-dik Madoqua kirkii Maloiy 1973 • Rock hyrax Procavia Rübsamen and capensis Kettembeil 1980 Desert • Arabian oryx Oryx leucoryx Ostrowski et al. 2003 • Fennec fox Vulpes zerda Noll-Banholzer 1979 Adaptive hypo- or Semidesert hyperthermia • Grant’s gazelle Nanger granti Taylor 1970b • Greater Egyptian jerboa El Hilali and Veillat Jaculus orientalis 1975 Desert • Camel Camelus dromedarius Grigg et al. 2009 • Jackrabbit Lepus Shoemaker et al. californicus 1976 Wide thermoneutral Semidesert zone • Littledale’s whistling rat Jackson et al. 2004 Parotomys littledalei • Tammar wallaby Macropus Kinnear et al. 1968 eugenii Desert • Allenby’s gerbil Gerbillus Haim 1984 allenbyi • Camel Camelus dromedarius Schmidt-Nielsen et al. 1967 Maintenance of Semidesert nonshivering • African lesser bushbaby Nowack et al. 2013 thermogenesis Galago moholi * Information in • African striped mouse Haim and Fourie large mammals is Rhabdomys pumilio 1980b lacking • Damara ground squirrel Haim et al. 1986 Xerus princeps Desert • Golden spiny mouse Kronfeld-Schor Acomys russatus et al. 2000 • Palestine mole rat Spalax Haim et al. 1984 ehrenbergi (chromosomal form 2n = 60)

continued

Table 2C Continued

Nature of Selected Present in my Degree of plasticity System the trait Trait Example species references study species? or flexibility?

Enters torpor (or Semidesert hibernation) • Grey mouse lemur Schmid 2001; * And/or in Microcebus murinus Schmid and response to food/ Speakman 2009 water restriction. • North African elephant Lovegrove et al. Information on shrew Elephantulus rozeti 2001 large mammals Desert is lacking in the • Round-tailed ground Hudson 1964 literature squirrel Spermophilus tereticaudus • Stripe-faced dunnart Song and Geiser Sminthopsis macroura 1997 Fixed Storage of body heat Semidesert during the day • Grant’s gazelle Nanger Taylor 1970a and dissipation at granti night • Little red kaluta Withers and Cooper * The terms Dasykaluta rosamondae 2009 “adaptive Desert heterothermy” • Sand gazelle Gazella Ostrowski and and marica Williams 2006 “heterothermy” • Harris’s antelope squirrel Osborn 1991 are also used Ammospermophilus harrisii Increased Semidesert erythrocyte • Guanaco Lama guanicoe Cornelius and circulation Kaneko 1962 efﬁciency; Desert erythrocyte • Camel Camelus Oyewale et al. 2011 volume ﬂexibility dromedarius and enhanced • Desert bighorn sheep Turner 1979 erythrocyte life Ovis canadensis nelsoni span * Information is lacking in small mammals and semidesert species Selective brain Semidesert cooling • Beisa oryx Oryx beisa Fuller et al. 2004 * The incidence is • Springbok Antidorcas Mitchell et al. 1997 lacking in the marsupialis literature, and is Desert debated in large • Arabian oryx Oryx leucoryx Hetem et al. 2012 mammals • Camel Camelus Elkhawad 1992 dromedarius Narrow but high Semidesert thermoneutral • African striped mouse Haim and Fourie zone Rhabdomys pumilio 1980a * Information in • Cape short-eared gerbil Downs and Perrin large mammals is Desmodillus auricularis 1994 lacking • Palmer’s chipmunk Lowrey and Tamias palmeri Longshore 2005 Desert • Naked-footed gerbil Haim 1984 Gerbillus nanus • Spiny mouse Acomys Perrin and Downs spinosissimus 1994

continued

Table 2C Continued

Nature of Selected Present in my Degree of plasticity System the trait Trait Example species references study species? or flexibility?

High thermal Semidesert conductance • African striped mouse Haim and Fairall Rhabdomys pumilio 1986 • Awassi sheep Ovis aries Degen and Shkolnik 1978 • Western barred bandicoot Larcombe and Perameles bougainville Withers 2006 bougainville Desert • Collared peccary Pecari Zervanos and tajacu Hadley 1973 • Desert kit fox Vulpes Golightly and macrotis arsipus Ohmart 1983 Morphology Flexible Limited Semidesert subcutaneous • Boer goat Capra aegagrus Casey and van fat deposition or hircus Niekerk 1988 localized storage • Fat-tailed dunnart Morton 1978 Sminthopsis crassicaudata Desert • Camel Camelus Young 1976 dromedarius • Soda Spring Valley Bartholomew and kangaroo mouse MacMillen 1961 Microdipodops pallidus Fixed Bipedal locomotion Semidesert (or tendency) • Great jerboa Allactaga Schmidt-Nielsen and major Schmidt-Nielsen 1952 • Tammar wallaby Macropus Baudinette et al. eugenii 1992 Desert • Dusky hopping mouse Schmidt-Nielsen and Notomys fuscus Schmidt-Nielsen 1952 • Red kangaroo Macropus Dawson and Taylor rufus 1973 Short coarse pelage Semidesert • African buffalo Syncerus Marai and Haeeb caffer 2010 • Gulf coast kangaroo rat Baumgardner 1991 Dipodomys compactus Desert • Arabian oryx Oryx leucoryx Stewart 1963 • Round-tailed ground Walsberg 1988 squirrel Spermophilus tereticaudus Light colored pelage Semidesert for reﬂecting • Panamint kangaroo rat Intress and Best solar radiation Dipodomys panamintinus 1990 and reducing heat • Springbok Antidorcas Mitchell et al. 1997 uptake marsupialis Desert • Desert bighorn sheep McCutchen 1981 Ovis canadensis nelsoni • Eastern Patagonian Giannoni et al. 2001 laucha Eligmodontia typus

continued

Table 2C Continued

Nature of Selected Present in my Degree of plasticity System the trait Trait Example species references study species? or flexibility?

Dark pigmented skin Semidesert • African buffalo Syncerus Marai and Haeeb caffer 2010 • African striped mouse Timm and Kermott Rhabdomys pumilio 1982 • Damara ground squirrel Waterman and Xerus princeps Herron 2004 Desert • Addax Addax Portas et al. 2003 nasomaculatus • Golden spiny mouse Haim and Rozenfeld Acomys russatus 1995 Presence of a carotid Semidesert rete • Kirk’s dik-dik Madoqua Kamau et al. 1984 * Information is kirkii lacking for small • Springbok Antidorcas Mitchell et al. 2002 mammals marsupialis Desert • Camel Camelus Elkhawad 1992 dromedarius • Pronghorn Antilocapra Mitchell et al. 2009 americana Nasal countercurrent Semidesert exchange system • Giraffe Giraffa Langman et al. 1979 * This concurrently camelopardalis provides a beneﬁt • Little red kaluta Withers and Cooper against water loss Dasykaluta rosamondae 2009 Desert • Camel Camelus Schmidt-Nielsen dromedarius et al. 1981b • Merriam’s kangaroo rat Jackson and Dipodomys merriami Schmidt-Nielsen 1964

Wingfield 2003). Whether this leads to per- ical markers can indicate a deviation from manent damage and pathology, and finally osmotic homeostasis, such as decreased death, can be modeled using the reactive plasma volume (Siebert and Macfarlane scope model, which takes into account the 1975; Ouajd and Kamel 2009) or increased short- and long-term effects of physiological concentration of proteins and sugars (Ouajd mediators of allostasis (Romero et al. 2009; and Kamel 2009). Metabolism is regulated Romero 2012). by corticosterone and thyroxine, mobiliz- Osmoregulation is regulated by the se- ing hepatic lipids and fatty acids in response cretion of several hormones, especially to food restriction (Ostrowski et al. 2006; AVP, aldosterone, and renin (Finberg et al. Ouajd and Kamel 2009). Thermoregulation 1978; Ben Goumi et al. 1993), which regu- is maintained by corticosterone, dexameth- late water reabsorption in the kidneys and asone, and prednisolone, as well as sodium, water excretion via urine. Several physiolog- and their influence on the sympathetic ner-

This content downloaded from 137.219.126.019 on May 31, 2016 18:08:34 PM All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c). June 2016 Species Resilience to Droughts 161 vous system (Maickel et al. 1967). Thermo- load (Mitchell et al. 2002). In sum, special- regulatory enhancements are indicated by ized adaptations are of little interest in es- increased erythrocyte circulation efficiency tablishing how a nondesert-adapted species and changes in erythrocyte volume flexibil- would respond to the increasing frequency ity (Ouajd and Kamel 2009), which would of droughts, because such species will not facilitate oxygen circulation in the body. have specialized adaptations. Third, morphological structures, both Traits that show adaptive developmen- internal and external, can help an animal tal plasticity can vary between individuals to cope with water and food shortage, as due to environmental factors. However, al- well as high Ta (Tables 2a, b, and c). Kid- though developmentally plastic traits are ney morphology, in particular long loops flexible during early life stages, they are of Henle, increases water reabsorption and generally fixed by adulthood (Piersma and minimizes water loss by increasing urine van Gils 2010). Adaptive developmental concentration (Ouajd and Kamel 2009). plasticity is thus an important determinant Organ size and volume can be altered in of resilience to drought. Essentially, every response to food restriction to minimize fixed trait can be categorized according the energetic costs of maintaining those or- to the nature and degree of its develop- gans (Ostrowski et al. 2006). Body size itself mental plasticity, also known as a reaction can have a profound effect on resilience to norm (Cassidy et al. 2014). This reaction climate, and can change both plastically or norm can be narrow, with a slope close to due to evolutionary adaptation (Brown and zero (totally fixed trait), or it can be broad. Brown 1998). In mammals, paleontologists Here, we include traits that show adaptive have observed dwarfing (reduction in body developmental plasticity as fixed traits, be- size) during the Paleocene-Eocene bound- cause they are not flexible in adults (Ta- ary, a period of global warming (Gingerich bles 2a, b, and c). As a consequence, to 2006), and dwarfing might also occur in determine the resilience to droughts by a extant mammals in response to increasing species, the level of adaptive developmen-

Ta. Similarly, pelage color and pattern, and tal plasticity of every fixed trait should be skin color can assist in thermoregulation, estimated. Broad adaptive developmental minimizing solar absorption and increas- plasticity indicates a greater likelihood that ing solar radiation (Stewart 1963; Haim a generation exposed to droughts during and Rozenfeld 1995). early development (or to environmental stimuli predicting droughts) will develop traits enabling resilience to droughts. how flexible is the trait? General adaptations evolve in response to fluctuating and dynamic selection pres- The final stage of the adaptive triquetra sures in multiple habitats and are likely to model is to establish the flexibility of the be common among most (if not all) mam- trait under increasing drought conditions mals. For example, all mammals secrete (Box 2). Specialized adaptations evolve AVP from the pituitary to regulate water in response to strong selection pressures reabsorption in the kidneys (Acher 1993). imposed by particular habitats. These ad- Many general adaptations are likely to be aptations are likely to be species-specific phenotypically flexible. Exaptations must because different species adopt different also be considered here because their uti- strategies, as well as a combination of strat- lization in the current context is flexible, egies, for survival and reproduction under even if the trait evolved as a specialized challenging environmental conditions. Fur- adaptation in another context. Recent thermore, these adaptations are relatively evidence from the available vertebrate lit- fixed, with limited flexibility. Specialized erature suggests that most phenotypic re- adaptations, such as the carotid rete uti- sponses to climate change and increased lized in brain cooling, enables individuals droughts would be due to the flexibility of some species to cope with increasing heat of traits (Canale and Henry 2010). There-

This content downloaded from 137.219.126.019 on May 31, 2016 18:08:34 PM All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c). 162 THE QUARTERLY REVIEW OF BIOLOGY Volume 91 fore, we suggest that identifying flexible a species, a detailed understanding of the traits representing general adaptations and biology and evolutionary history of the spe- exaptations of nondesert-adapted species is cies is the requisite first step prior to large- vital for determining whether a species has scale decision-making processes. the potential to persist under increasing One important aspect not covered by this drought conditions (Tables 2a, b, and c). process is the environment. By definition, drought occurs when the current precipitation falls significantly below the long-term mean Using the Adaptive Triquetra of a defined area, leading to water shortage to Estimate Species Resilience (Dai 2011). Thus, droughts can differ dramat- or Vulnerability to Drought ically in intensity and duration, and a population that can cope well with, for example, We have attempted to summarize all a 30% reduction of precipitation over a few known traits of the adaptive triquetra that months, might not survive a 60% reduction mammals could use to cope with droughts in precipitation over a longer period. In addi- (Tables 2a, b, and c). These can be used by tion, a population’s habitat may provide suit- ecologists and nature conservationists to able microclimatic refugia that could facilitate assess the resilience or vulnerability of one persistence, but not the habitat of another or several species to drought. These tables population of the same species. However, it reflect the variety of traits and species pos- is important to understand the complexity of sessing these traits. Currently, in most cases, the species first, and then focus on the envi- more research on a specific species would ronment and habitat later, as the biology of an be required by ecologists/nature conserva- animal will determine its vulnerability, while tionists to accurately estimate the resilience the modulating role of the environment may to drought by a particular species. The ta- promote or hinder resilience. bles enable a comparison to be made between different traits, as well as between different large- and/or small-bodied species. They provide a step-by-step approach Concluding Remarks: that could help in making decisions on con- The Importance of Flexibility servation action, especially of which species Phenotypic flexibility, rather than future to focus on, and which of the three stress- evolutionary adaptation, will most likely facili- ors is relevant. For example, for species A tate adaptive responses to climate change it might be most important to offer water and increased droughts in the short term at artificial water points during droughts, (Canale and Henry 2010), which in the although for species B food shortage could long term might lead to evolutionary ad- be more important, so supplemental food aptation (Lind et al. 2015; Scheiner et al. should be the priority. 2015). Identifying those traits that promote We have planned Tables 2a, b, and c in persistence in a period of change, as well such a manner that they can be directly as understanding the degree of their flex- applied. In the second to last column, one ibility, is crucial for assessing whether or can mark whether or not a specific trait is not a species will persist under increased present in a species. In the last column, the frequency and/or periodicity of droughts. flexibility of that trait for that species can In addition to flexibility, resilience might be estimated. These two columns provide also arise because of exaptation. The con- the first overview for a specific species and cept of exaptation has been criticized as will give some indication of how resilient or not being useful to understand how spe- vulnerable it could be. Nonetheless, we re- cies are successful in their current environ- alize that, in nearly all cases, filling in these ment (Larson et al. 2013). Yet, the concept tables will generate more questions than might be useful for understanding whether answer the critical question of how resilient and how species will be able to cope with a species is to droughts. Thus, one conclu- rapid global change because exaptations sion is that to assess drought resilience of could provide important benefits for spe-

This content downloaded from 137.219.126.019 on May 31, 2016 18:08:34 PM All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c). June 2016 Species Resilience to Droughts 163 cies not currently accustomed to drought could be present in species from nondes- conditions. ert environments, in contrast to specialized Phenotypic flexibility operates at the in- traits of desert species. Comparative assess- dividual rather than at the population level ment of these species will facilitate identifi- (Rymer et al. 2013), so the ability of species cation of traits that could provide fitness to cope with change will depend largely on advantages for other species encountering the flexibility of its individuals. In addition, increasingly drier conditions. Furthermore, individuals that persist and reproduce trans- although a species may have a suite of exist- mit genes for trait flexibility to their off- ing phenotypic adaptations or exaptations to spring, and flexibility can be a strong driver droughts, the interaction with other species of phenotypic evolution (Piersma and van in its environment, its habitat requirements, Gils 2010; Standen et al. 2014). Thus, in the amount of available habitat, and human mid to long term, these traits, as well as the persecution/exploitation will all influence ability to be flexible, could become fixed its persistence. Future empirical studies and through evolutionary adaptation, becoming conservation programs will test the useful- general or specialized adaptations. How- ness and applicability of the adaptive tri- ever, because phenotypic flexibility can be quetra and possibly modify it, enabling us to costly, it is important to study to what degree better predict which populations are vulner- those traits that are phenotypically flexible able to drought-related extinction. in order to establish the limits of this plasticity in promoting persistence. acknowledgments To understand which traits could promote species persistence to increased periodicity The suggestions provided by the editor and two anon- ymous reviewers greatly improved the manuscript. of droughts and increased aridification, we We are grateful for support by the University of the should focus on those species currently in- Witwatersrand (Neville Pillay), James Cook University habiting semideserts because they are likely (Tasmin L. Rymer), the Université de Strasbourg’s to possess a suite of existing traits that could Institute for Advanced Study (Carsten Schradin), and be advantageous during droughts and that the CNRS (Carsten Schradin).

References

Acher R. 1993. Neurohypophysial peptide systems: pro- Black R., Bennett S. R. G., Thomas S. M., Beddington cessing, machinery, hydroosmotic regulation, adap- J. R. 2011. Climate change: migration as adapta- tation and evolution. Regulatory Peptides 45:1–13. tion. Nature 478:447–449. Acocks J. P. H. 1988. Veld types of South Africa. Mem- Boroda R., Matmon A., Amit R., Haviv I., Arnold M., oirs of the Botanical Survey of South Africa 57:1–146. Aumaître G., Bourlès D. L., Keddadouche K., Eyal Alley R. B., Marotzke J., Nordhaus W. D., Overpeck Y., Enzel Y. 2014. Evolution and degradation of J. T., Peteet D. M., Pielke R. A. Jr., Pierrehumbert ﬂat-top mesas in the hyper-arid Negev, Israel re- R. T., Rhines P. B., Stocker T. F., Talley L. D., Wal- vealed from 10Be cosmogenic nuclides. Earth Sur- lace J. M. 2003. Abrupt climate change. Science face Processes and Landforms 39:1611–1621. 299:2005–2010. Bozinovic F., Contreras L. C. 1990. Basal rate of me- Baldwin J. M. 1896. A new factor in evolution. Ameri- tabolism and temperature regulation of two desert can Naturalist 30:441–451. herbivorous octodontid rodents: Octomys mimax Bale T. L. 2015. Epigenetic and transgenerational and Tympanoctomys barrerae. Oecologia 84:567–570. reprogramming of brain development. Nature Re- Breed M. F., Ottewell K. M., Gardner M. G., Lowe A. views Neuroscience 16:332–344. J. 2011. Clarifying climate change adaptation re- Baum D. A., Larson A. 1991. Adaptation reviewed: a sponses for scattered trees in modiﬁed landscapes. phylogenetic methodology for studying character Journal of Applied Ecology 48:637–641. macroevolution. Systematic Zoology 40:1–18. Brown C. R., Brown M. B. 1998. Intense natural se- Ben Goumi M., Riad F., Giry J., de la Farge F., Safwate lection on body size and wing and tail asymmetry A., Davicco M.-J., Barlet J.-P. 1993. Hormonal con- in cliff swallows during severe weather. Evolution trol of water and sodium in plasma and urine of 52:1461–1475. camels during dehydration and rehydration. Gen- Cahill A. E., Aiello-Lammens M. E., Fisher-Reid M. C., eral and Comparative Endocrinology 89:378–386. Hua X., Karanewsky C. J., Ryu H. Y., Sbeglia G. C.,

Spagnolo F., Waldron J. B., Warsi O., Wiens J. J. Dukas R. 1999. Costs of memory: ideas and predic- 2013. How does climate change cause extinction? tions. Journal of Theoretical Biology 197:41–50. Proceedings of the Royal Society B: Biological Sciences Elkhawad A. O. 1992. Selective brain cooling in desert 280:2012890. animals: the camel (Camelus dromedarius). Compar- Canale C. I., Henry P.-Y. 2010. Adaptive phenotypic ative Biochemistry and Physiology Part A: Physiology plasticity and resilience of vertebrates to increas- 101:195–201. ing climatic unpredictability. Climate Research Etterson J. R., Shaw R. G. 2001. Constraint to adaptive 43:135–147. evolution in response to global warming. Science Cassidy E. J., Bath E., Chenoweth S. F., Bondurian- 294:151–154. sky R. 2014. Sex-specific patterns of morpholog- Fahrig L. 2003. Effects of habitat fragmentation on ical diversification: evolution of reaction norms biodiversity. Annual Review of Ecology and Systematics and static allometries in neriid flies. Evolution 34:487–515. 68:368–383. Faye B. 1997. Le guide de l’élevage du dromadaire. Li- Champagne F. A. 2013. Epigenetics and developmen- bourne (France): Sanofi Santé Nutrition Animale. tal plasticity across species. Developmental Psychobi- Finberg J. P., Yagil R., Berlyne G. M. 1978. Response ology 55:33–41. of the renin-aldosterone system in the camel to Champagne F. A., Rissman E. F. 2011. Behavioral epi- acute dehydration. Journal of Applied Physiology 44: genetics: a new frontier in the study of hormones 926–930. and behavior. Hormones and Behavior 59:277–278. Galbraith H., Jones R., Park R., Clough J., Herrod- Charmandari E., Tsigos C., Chrousos G. 2005. Endo- Julius S., Harrington B., Page G. 2002. Global crinology of the stress response. Annual Review of climate change and sea level rise: potential los- Physiology 67:259–284. ses of intertidal habitat for shorebirds. Waterbirds Charmantier A., McCleery R. H., Cole L. R., Perrins C., 25:173–183. Kruuk L. E. B., Sheldon B. C. 2008. Adaptive phe- Ghalambor C. K., McKay J. K., Carroll S. P., Reznick notypic plasticity in response to climate change in D. N. 2007. Adaptive versus non-adaptive pheno- a wild bird population. Science 320:800–803. typic plasticity and the potential for contemporary Charney J., Quirk W. J., Chow S.-H., Kornfield J. adaptation in new environments. Functional Ecology 1977. A comparative study of the effects of albedo 21:394 – 407. change on drought in semi-arid regions. Journal of Gingerich P. D. 2006. Environment and evolution the Atmospheric Sciences 34:1366–1385. through the Paleocene-Eocene thermal maximum. Chaves M. M., Maroco J. P., Pereira J. S. 2003. Un- Trends in Ecology and Evolution 21:246–253. derstanding plant responses to drought—from Gomulkiewicz R., Houle D. 2009. Demographic and genes to the whole plant. Functional Plant Biology genetic constraints on evolution. American Natu 30:239–264. ralist 174:E218–E229. Chevin L.-M. 2013. Genetic constraints on adapta- Gonzalez A., Ronce O., Ferriere R., Hochberg M. E. tion to a changing environment. Evolution 67: 2013. Evolutionary rescue: an emerging focus at 708–721. the intersection between ecology and evolution. Coddington J. A. 1994. The roles of homology and Philosophical Transactions of the Royal Society B: Bio convergence in studies of adaptation. Pages 53–78 logical Sciences 368:20120404. in Phylogenetics and Ecology, edited by P. Eggleton Gould S. J., Lewontin R. C. 1979. The spandrels of San and R. I. Vane-Wright. Linnean Society Sympo- Marco and the Panglossian paradigm: a critique sium Series, Number 17. London (United King- of the adaptationist programme. Proceedings of the dom): Academic Press. Royal Society B: Biological Sciences 205:581–598. Dai A. 2011. Drought under global warming: a re- Gould S. J., Vrba E. S. 1982. Exaptation—a missing view. Wiley Interdisciplinary Reviews: Climate Change term in the science of form. Paleobiology 8:4–15. 2:45–65. Grubbs D. E. 1980. Tritiated water turnover in free- de Wit P., Palumbi S. R. 2013. Transcriptome-wide living desert rodents. Comparative Biochemistry and polymorphisms of red abalone (Haliotis rufescens) Physiology Part A: Physiology 66:89–98. reveal patterns of gene flow and local adaptation. Haim A., Rozenfeld F. M. 1995. Temporal segregation Molecular Ecology 22:2884 –2897. in co-existing Acomys species: the possible role of DeWitt T. J., Sih A., Wilson D. S. 1998. Costs and limits nest site. Journal of Arid Environments 29:505–509. of phenotypic plasticity. Trends in Ecology and Evo- Harley C. D. G. 2011. Climate change, keystone preda- lution 13:77–81. tion, and biodiversity loss. Science 334:1124 –1127. Dochtermann N. A., Schwab T., Sih A. 2015. The con- Hetem R. S., Strauss W. M., Fick L. G., Maloney S. K., tribution of additive genetic variation to personal- Meyer L. C. R., Fuller A., Shobrak M., Mitchell ity variation: heritability of personality. Proceedings D. 2012. Selective brain cooling in Arabian oryx of the Royal Society B: Biological Sciences 282:20142201. (Oryx leucoryx): a physiological mechanism for

coping with aridity? Journal of Experimental Biology Lewontin R. C. 1970. The units of selection. Annual 215:3917–3924. Review of Ecology and Systematics 1:1–18. Hodgson D., McDonald J. L., Hosken D. J. 2015. What Li Y., Ye W., Wang M., Yan X. 2009. Climate change do you mean, “resilient”? Trends in Ecology and Evo- and drought: a risk assessment of crop-yield im- lution 30:503–506. pacts. Climate Research 39:31–46. Hoffman J. 2014. Physiological response of Bufo viridis Lind M. I., Yarlett K., Reger J., Carter M. J., Becker- (Laurenti, 1768) populations across an aridity gra- man A. P. 2015. The alignment between pheno- dient. Alytes—International Journal of Batrachology typic plasticity, the major axis of genetic variation 30:33–41. and the response to selection. Proceedings of the Hoffmann A. A., Sgrò C. M. 2011. Climate change and Royal Society B: Biological Sciences 282:20151651. evolutionary adaptation. Nature 470:479–485. Maickel R. P., Stern D. N., Takabatake E., Brodie Hughes T. P., Rodrigues M. J., Bellwood D. R., B. B. 1967. The sympathetic nervous system as a Ceccarelli D., Hoegh-Guldberg O., McCook homeostatic mechanism. II. Effect of adrenocorti- L., Moltschaniwskyj N., Pratchett M. S., Steneck cal hormones on body temperature maintenance R. S., Willis B. 2007. Phase shifts, herbivory, and of cold-exposed adrenalectomized rats. Journal the resilience of coral reefs to climate change. Cur- of Pharmacology and Experimental Therapeutics 157: rent Biology 17:360–365. 111–116. IPCC 2007. Climate Change 2007: The Physical Science McCue M. D. 2010. Starvation physiology: reviewing Basis: Contribution of Working Group I to the Fourth the different strategies animals use to survive a Assessment Report of the Intergovernmental Panel on common challenge. Comparative Biochemistry and Climate Change, edited by S. D. Solomon, Q. M. Physiology Part A: Molecular and Integrative Physiology Manning, Z. Chen, M. Marquis, K. B. Averyt, M. 156:1–18. Tignor, and H. L. Miller. Cambridge (United King- McEwen B. S., Wingﬁeld J. C. 2003. The concept of al- dom): Cambridge University Press. lostasis in biology and biomedicine. Hormones and IPCC 2013. Climate Change 2013: The Physical Science Ba- Behavior 43:2–15. sis: Working Group I Contribution to the Fifth Assessment McNaughton S. J., Wallace L. L., Coughenour M. B. Report of the Intergovernmental Panel on Climate Change, 1983. Plant adaptation in an ecosystem context: ef- edited by T. F. Stocker, D. Qin, G. K. Plattner, M. fects of defoliation, nitrogen, and water on growth M. B. Tignor, S. K. Allen, J. Boschung, A. Nauels, Y. of an African C4 sedge. Ecology 64:307–318. Xia, V. Bex, and P. M. Midgley. Cambridge (United Meigs P. 1953. World distribution of arid and semi- Kingdom): Cambridge University Press. arid homoclimates. Pages 203–209 in Reviews of Re- Jablonka E., Lamb M. J. 2005. Evolution in Four Dimen- search on Arid Zone Hydrology. Arid Zone Research sions: Genetic, Epigenetic, Behavioral, and Symbolic Series, Volume 1. Paris (France): UNESCO. Variation in the History of Life. Cambridge (Massa- Mery F., Burns J. G. 2010. Behavioural plasticity: an in- chusetts): MIT Press. teraction between evolution and experience. Evolu- Jablonka E., Lamb M. J. 2007. Précis of Evolution tionary Ecology 24:571–583. in Four Dimensions. Behavioral and Brain Sciences Michel M. J., Chevin L.-M., Knouft J. H. 2014. Evo- 30:353–392. lution of phenotype-environment associations by Jackson D. C., Schmidt-Nielsen K. 1964. Countercur- genetic responses to selection and phenotypic rent heat exchange in the respiratory passages. plasticity in a temporally autocorrelated environ- Proceedings of the National Academy of Sciences of the ment. Evolution 68:1374 –1384. United States of America 51:1192–1197. Miller G. H., Fogel M. L., Magee J. W., Gagan M. K., Jackson T. P., Bennett N. C., Spinks A. C. 2004. Is the Clarke S. J., Johnson B. J. 2005. Ecosystem col- distribution of the arid-occuring otomyine rodents lapse in Pleistocene Australia and a human role in of southern Africa related to physiological adap- megafaunal extinction. Science 309:287–290. tation or refuge type? Journal of Zoology 264:1–10. Mitchell D., Laburn H. P., Nijland M. J. M., Zurovsky Lande R., Shannon S. 1996. The role of genetic varia- Y., Mitchell G. 1987. Selective brain cooling and tion in adaptation and population persistence in a survival. South African Journal of Science 83:598–604. changing environment. Evolution 50:434 – 437. Mitchell D., Maloney S. K., Jessen C., Laburn H. P., Larson G., Stephens P. A., Tehrani J. J., Layton R. H. Kamerman P. R., Mitchell G., Fuller A. 2002. Adap- 2013. Exapting exaptation. Trends in Ecology and tive heterothermy and selective brain cooling in Evolution 28:497–498. arid-zone mammals. Comparative Biochemistry and Ledón-Rettig C. C., Pfennig D. W., Nascone-Yoder Physiology Part B: Biochemistry and Molecular Biology N. 2008. Ancestral variation and the potential for 131:571–585. genetic accommodation in larval amphibians: im- Moritz C., Agudo R. 2013. The future of species un- plications for the evolution of novel feeding strate- der climate change: resilience or decline? Science gies. Evolution and Development 10:316–325. 341:504 –508.

Murren C. J., Auld J. R., Callahan H., Ghalambor integration in a series of trophic traits: tracing the C. K., Handelsman C. A., Heskel M. A., Kingsolver evolution of myrmecophagy in spiders (Araneae). J. G., Maclean H. J., Masel J., Maughan H., Pfen- Zoology 116:27–35. nig D. W., Reylea R. A., Seiter S., Snell-Rood E., Pianka E. R. 2011. Evolutionary Ecology. Seventh Edi- Steiner U. K., Schlichting C. D. 2015. Constraints tion. Austin (Texas): E. R. Pianka. on the evolution of phenotypic plasticity: limits Piersma T., Drent J. 2003. Phenotypic flexibility and and costs of phenotype and plasticity. Heredity the evolution of organismal design. Trends in Ecol 115:293–301. ogy and Evolution 18:228–233. Nash D. J., Engineering Group Working Party. 2012. Piersma T., Lindström Å. 1997. Rapid reversible changes Desert environments. Geological Society, London, En- in organ size as a component of adaptive behaviour. gineering Geology Special Publications 25:7–32. Trends in Ecology and Evolution 12:134 –138. Negus N. C., Berger P. J., Brown B. W. 1986. Micro- Piersma T., van Gils J. A. 2010. The Flexible Phenotype: tine population dynamics in a predictable environ- A Body-Centred Integration of Ecology, Physiology, and ment. Canadian Journal of Zoology 64:785–792. Behaviour. Oxford (United Kingdom): Oxford Nettle D., Bateson M. 2015. Adaptive developmental University Press. plasticity: what is it, how can we recognize it and Pimm S. L. 2009. Climate disruption and biodiversity. when can it evolve? Proceedings of the Royal Society B: Current Biology 19:R595–R601. Biological Sciences 282:20151005. Pinter A. J. 1994. Climatic factors, reproductive suc- Ockendon N., Baker D. J., Carr J. A., White E. C., Al- cess and population dynamics in the montane mond R. E. A., Amano T., Bertram E., Bradbury vole, Microtus montanus. University of Wyoming Na- R. B., Bradley C., Butchart S. H. M., Doswald N., tional Park Service Research Center Annual Report Foden W., Gill D. J. C., Green R. E., Sutherland 18:92–93. W. J., Tanner E. V. J., Pearce-Higgins J. W. 2014. Podos J., Southall J. A., Rossi-Santos M. R. 2004. Vocal Mechanisms underpinning climatic impacts on mechanics in Darwin’s finches: correlation of beak natural populations: altered species interactions gape and song frequency. Journal of Experimental Bi- are more important than direct effects. Global ology 207:607–619. Change Biology 20:2221–2229. Quintero I., Wiens J. J. 2013. Rates of projected cli- Oppenheimer M., Campos M., Warren R., Birkmann mate change dramatically exceed past rates of cli- J., Luber G., O’Neill B., Takahashi K. 2014. Emer- matic niche evolution among vertebrate species. gent risks and key vulnerabilities. Pages 1039–1099 Ecology Letters 16:1095–1103. in Climate Change 2014: Impacts, Adaptation, and Randall J. A. 1993. Behavioural adaptations of desert Vulnerability: Part A: Global and Sectoral Aspects: rodents (Heteromyidae). Animal Behaviour 45: Contribution of Working Group II to the Fifth Assess- 263–287. ment Report of the Intergovernmental Panel on Climate Reik W. 2007. Stability and flexibility of epigenetic Change. Cambridge (United Kingdom): Cam- gene regulation in mammalian development. Na- bridge University Press. ture 447:425–432. Ostrowski S., Williams J. B., Mésochina P., Sauerwein Rezende E. L., Diniz-Filho J. A. F. 2012. Phylogenetic H. 2006. Physiological acclimation of a desert an- analyses: comparing species to infer adaptations telope, Arabian oryx (Oryx leucoryx), to long-term and physiological mechanisms. Comphrensive Phys- food and water restriction. Journal of Comparative iology 2:639–674. Physiology B: Biochemical, Systems, and Environmental Rivers J. W., Liebl A. L., Owen J. C., Martin L. B., Betts Physiology 176:191–201. M. G. 2012. Baseline corticosterone is positively Ouajd S., Kamel B. 2009. Physiological particularities related to juvenile survival in a migrant passerine of dromedary (Camelus dromedarius) and experi- bird. Functional Ecology 26:1127–1134. mental implications. Scandinavian Journal of Labo- Robertson B. A., Rehage J. S., Sih A. 2013. Ecological ratory Animal Science 36:19–29. novelty and the emergence of evolutionary traps. Ozgul A., Tuljapurkar S., Benton T. G., Pemberton Trends in Ecology and Evolution 28:552–560. J. M., Clutton-Brock T. H., Coulson T. 2009. The Romero L. M. 2012. Using the reactive scope model to dynamics of phenotypic change and the shrinking understand why stress physiology predicts survival sheep of St. Kilda. Science 325:464 –467. during starvation in Galápagos marine iguanas. Ozgul A., Childs D. Z., Oli M. K., Armitage K. B., General and Comparative Endocrinology 176:296–299. Blumstein D. T., Olson L. E., Tuljapurkar S., Coul- Romero L. M., Dickens M. J., Cyr N. E. 2009. The son T. 2010. Coupled dynamics of body mass and reactive scope model—a new model integrating population growth in response to environmental homeostasis, allostasis, and stress. Hormones and change. Nature 466:482–485. Behavior 55:375–389. Pekár S., Michalko R., Korenko S., Šedo O., Lízna- Rymer T. L., Pillay N., Schradin C. 2013. Extinction rová E., Sentenská L., Zdráhal Z. 2013. Phenotypic or survival? Behavioral flexibility in response to

environmental change in the African striped Valladares F., Balaguer L., Martinez-Ferri E., Perez- mouse Rhabdomys. Sustainability 5:163–186. Corona E., Manrique E. 2002. Plasticity, instabil- Saccheri I. J., Rousset F., Watts P. C., Brakefield P. ity and canalization: is the phenotypic variation M., Cook L. M. 2008. Selection and gene flow on in seedlings of sclerophyll oaks consistent with a diminishing cline of melanic peppered moths. the environmental unpredictability of Mediter- Proceedings of the National Academy of Sciences of the ranean ecosystems? New Phytologist 156:457–467. United States of America 105:16212–16217. Van Buskirk J., Steiner U. K. 2009. The fitness costs of Sarma V. V. L. N., Krishna G. M., Malini B. H., Rao developmental canalization and plasticity. Journal K . N. 2001. Landuse/landcover change detection of Evolutionary Biology 22:852–860. through remote sensing and its climatic implica- Vicente-Serrano S. M., Gouveia C., Camarero J. J., Beg- tions in the Godavari delta region. Journal of the uería S., Trigo R., López-Moreno J. I., Azorín-Molina Indian Society of Remote Sensing 29:85–91. C., Pasho E., Lorenzo-Lacruz J., Revuelto J., Scheiner S. M., Gomulkiewicz R., Holt R. D. 2015. Morán-Tejeda E., Sanchez-Lorenzo A. 2013. Re- The genetics of phenotypic plasticity. XIV. Coevo- sponses of vegetation to drought time-scales across lution. American Naturalist 185:594 –609. global land biomes. Proceedings of the National Acad- Schradin C., Pillay N. 2005. Demography of the emy of Sciences of the United States of America 110: striped mouse (Rhabdomys pumilio) in the succu- 52–57. lent karoo. Mammalian Biology 70:84 –92. Viles H. A., Goudie A. S. 2013. Weathering in the cen- Schradin C., Krackow S., Schubert M., Keller C., tral Namib Desert, Namibia: controls, processes and Schradin B., Pillay N. 2007. Regulation of activity implications. Journal of Arid Environments 93:20–29. in desert-living striped mice: the importance of Walker B. H., Emslie R. H., Owen-Smith R. N., Scholes basking. Ethology 113:606–614. R. J. 1987. To cull or not to cull: lessons from a Seager R., Tang M., Held I., Kushnir Y., Lu J., Vec- southern African drought. Journal of Applied Ecology chi G., Huang H.-P., Harnik N., Leetmaa A., Lau 24:381–401. N.-C., Li C., Velez J., Naik N. 2007. Model projec- Ward D. 2009. Morphological, physiological, and tions of an imminent transition to a more arid cli- behavioural adaptations of desert animals to the mate in southwestern North America. Science 316: abiotic environment. Pages 66–101 in The Biology 1181–1184. of Deserts, by D. Ward. Oxford (United Kingdom): Siebert B. D., Macfarlane W. V. 1975. Dehydration Oxford University Press. in desert cattle and camels. Physiological Zoology Webb J. K., Letnic M., Jessop T. S., Dempster T. 2014. 48:36 – 48. Behavioural flexibility allows an invasive vertebrate Sih A., Ferrari M. C. O., Harris D. J. 2011. Evolution to survive in a semi-arid environment. Biology Let- and behavioural responses to human-induced ters 10:20131014. rapid environmental change. Evolutionary Applica- West-Eberhard M. J. 1989. Phenotypic plasticity and tions 4:367–387. the origins of diversity. Annual Review of Ecology and Smit B., Burton I., Klein R. J. T., Wandel J. 2000. An Systematics 20:249–278. anatomy of adaptation to climate change and vari- Williams J. B., Ostrowski S., Bedin E., Ismail K. 2001. ability. Climate Change 45:223–251. Seasonal variation in energy expenditure, water Sperry J. H., Weatherhead P. J. 2008. Prey-mediated flux and food consumption of Arabian oryx Oryx effects of drought on condition and survival of a leucoryx. Journal of Experimental Biology 204:2301– terrestrial snake. Ecology 89:2770–2776. 2311. Standen E. M., Du T. Y., Larsson H. C. E. 2014. De- Williams S. E., Shoo L. P., Isaac J. L., Hoffmann A. A., velopmental plasticity and the origin of tetrapods. Langham G. 2008. Towards an integrated frame- Nature 513:54–58. work for assessing the vulnerability of species to Steiner U. K., Van Buskirk J. 2008. Environmental climate change. PLOS Biology 6:e325. stress and the costs of whole-organism phenotypic Willmer P., Stone G., Johnson I. 2000. Environmental plasticity in tadpoles. Journal of Evolutionary Biology Physiology of Animals. Malden (Massachusetts): 21:97–103. Blackwell Science. Stewart D. R. M. 1963. The Arabian oryx (Oryx leucoryx Wingfield J. C. 2013. The comparative biology of Pallas). African Journal of Ecology 1:103–117. environmental stress: behavioural endocrinol- Tanentzap A. J., Lee W. G., Schulz K. A. C. 2013. ogy and variation in ability to cope with novel, Niches drive peaked and positive relationships be- changing environments. Animal Behaviour 85: tween diversity and disturbance in natural ecosys- 1127–1133. tems. Ecosphere 4:133. Ylönen H., Ronkainen H. 1994. Breeding suppres- Taylor C. R. 1970. Dehydration and heat: effects on sion in the bank vole as antipredatory adaptation temperature regulation of East African ungulates. in a predictable environment. Evolutionary Ecology American Journal of Physiology 219:1136–1139. 8:658–666.

Yousef M. K., Johnson H. D. 1975. Thyroid activ- Zhang Z.-Q., Wang D.-H. 2007. Seasonal changes in ity in desert rodents: a mechanism for lowered thermogenesis and body mass in wild Mongolian metabolic rate. American Journal of Physiology gerbils (Meriones unguiculatus). Comparative Bio- 229:427–431. chemistry and Physiology Part A: Molecular and Inte- Zhang Y. M., Chen Y. N., Pan B. R. 2005. Distribution grative Physiology 148:346–353. and ﬂoristics of desert plant communities in the lower reaches of Tarim River, southern Xinjiang, People’s Republic of China. Journal of Arid Environ- Associate Editor: Andrew Sih ments 63:772–784. Handling Editor: John J. Wiens

Appendix 1 References associated with Tables 1, 2a, 2b, and 2c

Alagaili A. N., Mohammed O. B., Bennett N. C., urine osmolality and kidney water channels in Oosthuizen M. K. 2013. A tale of two jirds: the free-living degus: molecular mechanisms, physio- locomotory activity patterns of the King jird logical processes and ecological implications. Jour- (Meriones rex) and Lybian jird (Meriones lybicus) nal of Experimental Biology 206:2959–2966. from Saudi Arabia. Journal of Arid Environments Bradford D. F. 1974. Water stress of free-living Peromy- 88:102–112. scus truei. Ecology 55:1407–1414. Albert S. K., Krausman P. R. 1993. Desert mule deer Brown J. H., Munger J. C. 1985. Experimental manip- and forage resources in Southwest Arizona. South- ulation of a desert rodent community: food addi- western Naturalist 38:198–205. tion and species removal. Ecology 66:1545–1563. Aulagnier S., Granjon L., Shenbrot G., Bukhnikash- Buffenstein R. 1984. Energy and water balance during vili A. 2008. Meriones libycus. IUCN 2014. IUCN torpor and hydropenia in the pigmy gerbil, Ger- Red List of Threatened Species, Version 2014.3. billus pusillus. Journal of Comparative Physiology B: http://www.iucnredlist.org. (Accessed 3 Decem- Biochemical, Systems, and Environmental Physiology ber 2014). 154:535–544. Bartholomew G. A., MacMillen R. E. 1961. Oxygen Buffenstein R. 1985. The effect of a high fibre diet consumption, estivation, and hibernation in the on energy and water balance in two Namib desert kangaroo mouse, Microdipodops pallidus. Physiolog- rodents. Journal of Comparative Physiology B: Bio- ical Zoology 34:177–183. chemical, Systems, and Environmental Physiology Baudinette R. V., Snyder G. K., Frappell P. B. 1992. En- 155:211–218. ergetic cost of locomotion in the Tammar wallaby. Buffenstein R., Campbell W. E., Jarvis J. U. M. 1985. American Journal of Physiology: Regulatory, Integrative Identification of crystalline allantoin in the urine and Comparative Physiology 262:R771–R778. of African Cricetidae (Rodentia) and its role in Baumgardner G. D. 1991. Dipodomys compactus. Mam- their water economy. Journal of Comparative Physiol- malian Species 369:1–4. ogy B: Biochemical, Systems, and Environmental Physi- Ben Goumi M., Riad F., Giry J., de la Farge F., Safwate ology 155:493–499. A., Davicco M.-J., Barlet J.-P. 1993. Hormonal con- Bukovetzky E., Fares F., Schwimmer H., Haim A. 2012. trol of water and sodium in plasma and urine of Reproductive and metabolic responses of desert camels during dehydration and rehydration. Gen- adapted common spiny male mice (Acomys cahiri- eral and Comparative Endocrinology 89:378–386. nus) to vasopressin treatment. Comparative Biochem- Bennett A. F., Huey R. B., John-Alder H., Nagy K. A. istry and Physiology Part A: Molecular and Integrative 1984. The parasol tail and thermoregulatory be- Physiology 162:349–356. havior of the Cape ground squirrel Xerus inauris. Cain J. W. III, Krausman P. R., Rosenstock S. S., Turner Physiological Zoology 57:57–62. J. C. 2006. Mechanisms of thermoregulation and Bothma J. du P., Riche E. A. N. le. 1984. Aspects of the water balance in desert ungulates. Wildlife Society ecology and the behaviour of the leopard Panthera Bulletin 34:570–581. pardus in the Kalahari desert. Koedoe Supplement Carpenter R. E. 1966. A comparison of thermoregu- (1984):259–279. lation and water metabolism in the kangaroo rats Bozinovic F., Contreras L. C. 1990. Basal rate of me- Dipodomys agilis and Dipodomys merriami. University tabolism and temperature regulation of two desert of California Publications in Zoology 78:1–36. herbivorous octodontid rodents: Octomys mimax Carpenter R. E., Graham J. B. 1967. Physiological and Tympanoctomys barrerae. Oecologia 84:567–570. responses to temperature in the long-nosed bat, Bozinovic F., Gallardo P. A., Visser G. H., Cortés A. Leptonycteris sanborni. Comparative Biochemistry and 2003. Seasonal acclimatization in water flux rate, Physiology 22:709–722.

Casey N. H., van Niekerk W. A. 1988. The Boer goat. rongeurs, dont deux espèces d’habitat désertique. I. Origin, adaptability, performance testing, repro- Journal of Physiology 58:309–322. duction and milk production. Small Ruminant Re- Deblinger R. D., Alldredge A. W. 1989. Management search 1:291–302. implications of variations in pronghorn social be- Castel M., Abraham M. 1972. Effects of a dry diet on havior. Wildlife Society Bulletin 17:82–87. the antidiuretic hormone content of the neurohy- Degen A. A. 1977. Fat-tailed Awassi and German mut- pophysis in spiny mice as compared to the albino ton merino sheep under semi-arid conditions. 1. rat and mouse. General and Comparative Endocrinol- Total body water, its distribution and water turn- ogy 19:48–55. over. Journal of Agricultural Science 88:693–698. Chappell M. A., Bartholomew G. A. 1981a. Activity Degen A. A., Shkolnik A. 1978. Thermoregulation in and thermoregulation of the antelope ground fat-tailed Awassi, a desert sheep, and in German squirrel Ammospermophilus leucurus in winter and mutton merino, a mesic sheep. Physiological Zoology summer. Physiological Zoology 54:215–223. 51:333–339. Chappell M. A., Bartholomew G. A. 1981b. Standard Dereje M., Udén P. 2005. The browsing dromedary operative temperatures and thermal energetics of camel. I. Behaviour, plant preference and quality the antelope ground squirrel Ammospermophilus of forage selected. Animal Feed Science and Technol- leucurus. Physiological Zoology 54:81–93. ogy 121:297–308. Chen X., Dickman C. R., Thompson M. B. 1998. Diet Dexter N. 2003. The influence of pasture distribution, of the mulgara, Dasycercus cristicauda (Marsupialia: and temperature on adult body weight of feral Dasyuridae), in the Simpson Desert, central Aus- pigs in a semi-arid environment. Wildlife Research tralia. Wildlife Research 25:233–242. 30:75–79. Christian D. P. 1978. Effects of humidity and body size Diaz G. B., Ojeda R. A. 1999. Kidney structure and on evaporative water loss in three desert rodents. allometry of Argentine desert rodents. Journal of Comparative Biochemistry and Physiology Part A: Phys- Arid Environments 41:453 – 461. iology 60:425–430. Donadio E., Buskirk S. W., Novaro A. J. 2012. Ju- Christian D. P. 1980. Vegetative cover, water resources, venile and adult mortality patterns in a vicuña and microdistributional patterns in a desert rodent (Vicugna vicugna) population. Journal of Mammal- community. Journal of Animal Ecology 49:807–816. ogy 93:1536–1544. Cornelius C. E., Kaneko J. J. 1962. Erythrocyte life Downs C. T., Perrin M. R. 1990. The effect of diet on span in the guanaco. Science 137:673–674. water and energy turnover rates of four Gerbillurus Curtis B. A., Perrin M. R. 1979. Food preference of species in captivity. Journal of Zoology 222:215–233. the vlei rat (Otomys irroratus) and the four-striped Downs C. T., Perrin M. R. 1991. Urinary concentrating mouse (Rhabdomys pumilio). South African Journal of ability of four Gerbillurus species of southern Africa Zoology 14:224 – 229. arid regions. Journal of Arid Environments 20:71–81. Cypher B. L. 2003. Foxes (Vulpes species, Urocyon spe- Downs C. T., Perrin M. R. 1994. Comparative aspects of cies, and Alopex lagopus). Pages 511–546 in Wild the thermal biology of the short-tailed gerbil, Des- Mammals of North America: Biology, Management, and modillus auricularis, and the bushveld gerbil, Tatera Conservation, edited by G. A. Feldhamer, B. C. leucogaster. Journal of Thermal Biology 19:385–392. Thompson, and J. A. Chapman. Second Edition. du Plessis A., Kerley G. I. H., deo Winter P. E. 1992. Baltimore (Maryland): Johns Hopkins University Refuge microclimates of rodents: a surface nesting Press. Otomys unisulcatus and a burrowing Parotomys bran- Daly M., Daly S. 1973. On the feeding ecology of tsii. Acta Theriologica 37:351–358. Psammomys obesus (Rodentia: Gerbillinae) in Wadi Ehrhardt N., Heldmaier G., Exner C. 2005. Adaptive Saoura, Algeria. Mammalia 37:545–561. mechanisms during food restriction in Acomys rus- Dawson T. J., Brown G. D. 1970. A comparison of satus: the use of torpor for desert survival. Journal the insulative and reflective properties of the fur of Comparative Physiology B: Biochemical, Systems, and of desert kangaroos. Comparative Biochemistry and Environmental Physiology 175:193–200. Physiology 37:23–38. El-Hadi H. M. 1986. The effect of dehydration on Su- Dawson T. J., Taylor C. R. 1973. Energetic cost of loco- danese desert sheep and goats. Journal of Agricul- motion in kangaroos. Nature 246:313–314. tural Science 106:17–20. Dawson T. J., Denny M. J. S., Russell E. M., Ellis B. El Hilali M., Veillat J.-P. 1975. Jaculus orientalis: a true 1975. Water usage and diet preferences of free hibernator. Mammalia 39:401–404. ranging kangaroos, sheep and feral goats in the El Ouezzani S., Lafon P., Tramu G., Magoul R. 2001. Australian arid zone during summer. Journal of Zo- Neuropeptide Y gene expression in the jerboa ology 177:1–23. arcuate nucleus: modulation by food deprivation de Rouffignac C., Morel F. 1965. Etude comparée du and relationship with hibernation. Neuroscience Let- renouvellement de l’eau chez quatre espèces de ters 305:127–130.

Elkhawad A. O. 1992. Selective brain cooling in des- intake, digestibility and nitrogen utilization by ert animals: the camel (Camelus dromedarius). Com- camels compared to sheep and goats fed low pro- parative Biochemistry and Physiology Part A: Physiology tein desert by-products. Options Méditerranéennes— 101:195–201. Série Séminaires 2:75–81. Emmanuel B., Howard B. R., Emady M. 1976. Urea Gilad O., Grant W. E., Saltz D. 2008. Simulated dy- degradation in the camel. Canadian Journal of Ani- namics of Arabian oryx (Oryx leucoryx) in the Is- mal Science 56:595–601. raeli Negev: effects of migration corridors and Faye B. 1997. Le guide de l’élevage du dromadaire. Li- post-reintroduction changes in natality on popula- bourne (France): Sanoﬁ Santé Nutrition Animale. tion viability. Ecological Modelling 210:169–178. Fielden L. J., Perrin M. R., Hickman G. C. 1990. Water Golightly R. T. Jr., Ohmart R. D. 1983. Metabolism and metabolism in the Namib Desert golden mole, Er- body temperature of two desert canids: coyotes emitalpa granti namibensis (Chrysochloridae). Com- and kit foxes. Journal of Mammalogy 64:624 –635. parative Biochemistry and Physiology Part A: Physiology Grigg G., Beard L., Dörges B., Heucke J., Coven- 96:227–234. try J., Coppock A., Blomberg S. 2009. Strategic Finberg J. P., Yagil R., Berlyne G. M. 1978. Response of (adaptive) hypothermia in bull dromedary camels the renin-aldosterone system in the camel to acute during rut; could it increase reproductive success? dehydration. Journal of Applied Physiology 44:926 –930. Biology Letters 5:853–856. Fourie F. le R., Haim A. 1980. Enzymatic activity of Grubbs D. E. 1980. Tritiated water turnover in free- rodents acclimated to cold and long scotophase. living desert rodents. Comparative Biochemistry and International Journal of Biometeorology 24:237–241. Physiology Part A: Physiology 66:89–98. Frean J. L., Downs C. T., Lovegrove B. G. 1998. Osmo- Gutman R., Choshniak I., Kronfeld-Schor N. 2006. regulatory capacity of an arboreal rodent Thallomys Defending body mass during food restriction in nigricauda. Journal of Arid Environments 40:97–107. Acomys russatus: a desert rodent that does not store Fuller A., Maloney S. K., Mitchell G., Mitchell D. 2004. food. American Journal of Physiology: Regulatory, Inte- The eland and the oryx revisited: body and brain grative and Comparative Physiology 290:R881–R891. temperatures of free-living animals. International Gutman R., Hacmon-Keren R., Choshniak I., Kronfeld- Congress Series 1275:275–282. Schor N. 2008. Effect of food availability and Fuller A., Kamerman P. R., Maloney S. K., Matthee leptin on the physiology and hypothalamic gene A., Mitchell G., Mitchell D. 2005. A year in the expression of the golden spiny mouse: a desert thermal life of a free-ranging herd of springbok rodent that does not hoard food. American Journal Antidorcas marsupialis. Journal of Experimental Biology of Physiology: Regulatory, Integrative and Comparative 208:2855–2864. Physiology 295:R2015–R2023. Funston P. J., Skinner J. D., Dott H. M. 1994. Seasonal Haim A. 1984. Adaptive variations in heat production variation in movement patterns, home range and within gerbils (genus Gerbillus) from different hab- habitat selection of buffaloes in a semi-arid habi- itats. Oecologia 61:49–52. tat. African Journal of Ecology 32:100–114. Haim A., Borut A. 1981. Heat production and dissipa- Geiser F. 2010. Aestivation in mammals and birds. tion in golden spiny mice, Acomys russatus from two Pages 95–111 in Aestivation: Molecular and Physio- extreme habitats. Journal of Comparative Physiology logical Aspects, edited by C. A. Navas and J. E. Car- B: Biochemical, Systems, and Environmental Physiology valho. Berlin (Germany): Springer. 142:445–450. Geiser F., Pavey C. R. 2007. Basking and torpor in a Haim A., Fairall N. 1986. Geographical variations in rock-dwelling desert marsupial: survival strategies heat production and dissipation within two pop- in a resource-poor environment. Journal of Compar- ulations of Rhabdomys pumilio (Muridae). Compar- ative Physiology B: Biochemical, Systems, and Environ- ative Biochemistry and Physiology Part A: Physiology mental Physiology 177:885–892. 84:111–112. Ghobrial L. I. 1970. The water relations of the desert Haim A., Fourie F. le R. 1980a. Heat production in antelope Gazella dorcas dorcas. Physiological Zoology nocturnal (Praomys natalensis) and diurnal (Rhab- 43:249–256. domys pumilio) South African murids. South African Giannoni S. M., Dacar M., Taraborelli P., Borghi C. E. Journal of Zoology 15:91–94. 2001. Seed hoarding by rodents of the Monte Des- Haim A., Fourie F. le R. 1980b. Heat production in ert, Argentina. Austral Ecology 26:259–263. cold and long scotophase acclimated and winter Giannoni S. M., Borghi C. E., Dacar M., Campos acclimatized rodents. International Journal of Biome- C. M. 2005. Main food categories in diets of sigmo- teorology 24:231–236. dontine rodents in the Monte (Argentina). Masto- Haim A., Izhaki I. 1993. The ecological signiﬁcance zoología Neotropical 12:181–187. of resting metabolic rate and non-shivering ther- Gihad El S. A., El Gallad T. T., Sooud A. E. O., Abou mogenesis for rodents. Journal of Thermal Biology El Nasr H. M., Farid M. F. A. 1989. Feed and water 18:71–81.

Haim A., Rozenfeld F. M. 1995. Temporal segregation Hochman V., Kotler B. P. 2006. Effects of food quality, in co-existing Acomys species: the possible role of diet preference and water on patch use by Nubian nest site. Journal of Arid Environments 29:505–509. ibex. Oikos 112:547–554. Haim A., Heth G., Avnon Z., Nevo E. 1984. Adaptive Hoppe P. P. 1977. Comparison of voluntary food and physiological variation in nonshivering thermo- water consumption and digestion in Kirk’s dikdik genesis and its signiﬁcance in speciation. Journal and suni. African Journal of Ecology 15:41–48. of Comparative Physiology B: Biochemical, Systems, and Howell A. B., Gersh I. 1935. Conservation of water by Environmental Physiology 154:145–147. the rodent Dipodomys. Journal of Mammalogy 16:1–9. Haim A., Pelaot I., Sela A. 1986. Comparison of eco- Hudson J. W. 1964. Temperature regulation in the physiological parameters between two Apodemus round-tailed ground squirrel, Citellus tereticaudus. species coexisting in the same habitat. Pages 33–40 Annales Academiae Scientiarum Fennicae, Series A IV in Environmental Quality and Ecosystem Stability, Vol- 71:217–233. ume III A/B, edited by Z. Dubinsky and Y. Stein- Hulbert A. J., Dawson T. J. 1974. Thermoregulation berger. Ramat-Gan (Israel): Bar-Ilan University in perameloid marsupials from different environ- Press. ments. Comparative Biochemistry and Physiology Part Haines H., Macfarlane W. V., Setchell C., Howard B. A: Physiology 47:591–616. 1974. Water turnover and pulmocutaneous evap- Hulbert A. J., Hinds D. S., MacMillen R. E. 1985. Min- oration of Australian desert dasyurids and murids. imal metabolism, summit metabolism and plasma American Journal of Physiology 227:958–963. thyroxine in rodents from different environments. Hansen M. C. 1982. Desert bighorn sheep: another Comparative Biochemistry and Physiology Part A: Phys- view. Wildlife Society Bulletin 10:133–140. iology 81:687–693. Hartman L. A., Morton M. L. 1973. Plasma volume Hume J. D., Rübsamen K., Engelhardt W. V. 1980. Ni- changes in ground squirrels during water depriva- trogen metabolism and urea kinetics in the rock tion. Comparative Biochemistry and Physiology Part A: hyrax (Procavia habessinica). Journal of Comparative Physiology 46:79–94. Physiology B: Biochemical, Systems, and Environmental Hatough-Bouran A. 1990. The burrowing habits of de- Physiology 138:307–314. sertic rodents Jaculus jaculus and Gerbillus dasyurus Ilan M., Yom-Tov Y. 1990. Diel activity pattern of a di- in the Shaumari Reserve in Jordan. Mammalia urnal desert rodent, Psammomys obesus. Journal of 54:341–359. Mammalogy 71:66–69. Heimeier R. A., Donald J. A. 2006. The response of Intress C., Best T. L. 1990. Dipodomys panamintinus. the natriuretic peptide system to water deprivation Mammalian Species 354:1–7. in the desert rodent, Notomys alexis. Comparative Jaber L. S., Habre A., Rawda N., Abi Said M., Barbour Biochemistry and Physiology Part A: Molecular and In- E. K., Hamadeh S. 2004. The effect of water restric- tegrative Physiology 143:193–201. tion on certain physiological parameters in Awassi Hetem R. S., Strauss W. M., Fick L. G., Maloney S. K., sheep. Small Ruminant Research 54:115–120. Meyer L. C. R., Shobrak M., Fuller A., Mitchell D. Jaber L. S., Hanna N., Barbour E. K., Abi Said M., 2010. Variation in the daily rhythm of body tem- Rawda N., Chedid M., Hamadeh S. K. 2011. Fat perature of free-living Arabian oryx (Oryx leuco- mobilization in water restricted Awassi ewes sup- ryx): does water limitation drive heterothermy? plemented with vitamin C. Journal of Arid Environ- Journal of Comparative Physiology B: Biochemical, Sys- ments 75:625–628. tems, and Environmental Physiology 180:1111–1119. Jackson D. C., Schmidt-Nielsen K. 1964. Countercur- Hetem R. S., Strauss W. M., Heusinkveld B. G., de Bie S., rent heat exchange in the respiratory passages. Prins H. H. T., van Wieren S. E. 2011. Energy advan- Proceedings of the National Academy of Sciences of the tages of orientation to solar radiation in three Afri- United States of America 51:1192–1197. can ruminants. Journal of Thermal Biology 36:452–460. Jackson T. P., Bennett N. C., Spinks A. C. 2004. Is Hetem R. S., Strauss W. M., Fick L. G., Maloney S. K., the distribution of the arid-occurring otomyine Meyer L. C. R., Fuller A., Shobrak M., Mitchell rodents of southern Africa related to physiologi- D. 2012. Selective brain cooling in Arabian oryx cal adaptation or refuge type? Journal of Zoology (Oryx leucoryx): a physiological mechanism for 264:1–10. coping with aridity? Journal of Experimental Biology Kaißling B., de Roufﬁgnac C., Barrett J. M., Kriz W. 215:3917–3924. 1975. The structural organization of the kidney of Hinds D. S., MacMillen R. E. 1985. Scaling of energy the desert rodent Psammomys obesus. Anatomy and metabolism and evaporative water loss in hetero- Embryology 148:121–143. myid rodents. Physiological Zoology 58:282–298. Kam M., Degen A. A. 1993. Effect of dietary pre- Hinton H. E., Dunn A. M. S. 1967. Mongooses: Their formed water on energy and water budgets of two Natural History and Behaviour. Edinburgh (United sympatric desert rodents, Acomys russatus and Aco- Kingdom): Oliver & Boyd. mys cahirinus. Journal of Zoology 231:51–59.

Kamau J. M. Z., Maina J. N., Maloiy G. M. O. 1984. Larcombe A. N., Withers P. C. 2006. Thermoregula- The design and the role of the nasal passages in tory, metabolic and ventilatory physiology of the temperature regulation in the dik-dik antelope western barred bandicoot (Perameles bougainville (Rhynchotragus kirki) with observations on the ca- bougainville) in summer and winter. Australian Jour- rotid rete. Respiration Physiology 56:183–194. nal of Zoology 54:15–21. Kataria N., Kataria A. K. 2006. Endocrine and meta- Leggett K. E. A. 2004. Coprophagy and unusual thermo- bolic responses of Marwari sheep in arid tract. Slo- regulatory behaviour in desert-dwelling elephants of venian Veterinary Research 43:135–142. north-western Namibia. Pachyderm 36:113–115. Kennedy P. M., Hume I. D. 1978. Recycling of urea ni- Lewis R. E., Lewis J. H., Harrison D. L. 1965. On a col- trogen to the gut of the tammar wallaby (Macropus lection of mammals from northern Saudi Arabia. eugenii). Comparative Biochemistry and Physiology Part Proceedings of the Zoological Society of London 144:61–74. A: Physiology 61:117–121. Lovegrove B. G., Raman J., Perrin M. R. 2001. Daily Khachadurian A. K., Adrouni B., Yacoubian H. 1966. torpor in elephant shrews (Macroscelidea: Ele- Metabolism of adipose tissue in the fat tail of the phantulus spp.) in response to food deprivation. sheep in vivo. Journal of Lipid Research 7:427–436. Journal of Comparative Physiology B: Biochemical, Sys- Khalil F., Tawﬁc J. 1963. Some observations on the tems, and Environmental Physiology 171:11–21. kidney of the desert J. jaculus and G. gerbillus and Lowrey C., Longshore K. 2005. Long Term Conserva- their possible bearing on the water economy of tion Strategy for Palmers Chipmunk (Tamias palmeri) these animals. Journal of Experimental Zoology Part within the Spring Mountains, Nevada. Henderson A 154:259–271. (Nevada): United States Geological Survey. Khan M. S., Ghosh P. K., Sasidharan T. O. 1978. Effect Lubbe A. 2013. Thermoregulatory plasticity in of acute water restriction on plasma proteins and free-ranging vervet monkeys (Chlorocebus pygeryth- on blood and urinary electrolytes in Barmer goats rus). [MSc. thesis]. Johannesburg (South Africa): of the Rajasthan desert. Journal of Agricultural Sci- University of the Witwatersrand. ence 91:395–398. Macfarlane W. V., Morris R. J. H., Howard B. 1963. Turn- King J. M., Kingaby G. P., Colvin J. G., Heath B. R. over and distribution of water in desert camels, 1975. Seasonal variation in water turnover by oryx sheep, cattle and kangaroos. Nature 197:270–271. and eland on the Galana Game Ranch Research MacMillen R. E. 1965. Aestivation in the cactus Project. African Journal of Ecology 13:287–296. mouse, Peromyscus eremicus. Comparative Biochemistry Kinnear J. E., Purohit K. G., Main A. R. 1968. The abil- and Physiology 16:227–248. ity of the tammar wallaby (Macropus eugenii, Marsu- MacMillen R. E., Lee A. K. 1967. Australian desert pialia) to drink sea water. Comparative Biochemistry mice: independence of exogenous water. Science and Physiology 25:761–782. 158:383–385. Koford C. B. 1968. Peruvian desert mice: water inde- MacMillen R. E., Lee A. K. 1969. Water metabolism of pendence, competition, and breeding cycle near Australian hopping mice. Comparative Biochemistry the equator. Science 160:552–553. and Physiology 28:493–514. Kronfeld-Schor N., Haim A., Dayan T., Zisapel N., Maloiy G. M. O. 1972. Comparative physiology of des- Klingenspor M., Heldmaier G. 2000. Seasonal ert animals. Symposia of the Zoological Society of Lon- thermogenic acclimation of diurnally and noc- don 31:243–259. turnally active desert spiny mice. Physiological and Maloiy G. M. O. 1973. The water metabolism of a Biochemical Zoology 73:37–44. small East African antelope: the dik-dik. Proceedings Krysl L. J., Sowell B. F., Hubbert M. E., Plumb G. E., Jewett of the Royal Society B: Biological Sciences 184:167–178. T. K., Smith M. A., Waggoner J. W. 1984. Horses and Maloiy G. M. O., Rugangazi B. M., Clemens E. T. 1988. cattle grazing in the Wyoming red desert. II. Dietary Physiology of the dik-dik antelope. Comparative quality. Journal of Range Management 37:252–255. Biochemistry and Physiology Part A: Physiology 91:1–8. Laden S., Nehmadi L., Yagil R. 1987. Dehydration tol- Maloney S. K., Moss G., Cartmell T., Mitchell D. 2005. erance in Awassi fat-tailed sheep. Canadian Journal Alteration in diel activity patterns as a thermoreg- of Zoology 65:363–367. ulatory strategy in black wildebeest (Connochaetes Lagos V. O., Bozinovic F., Contreras L. C. 1995. Micro- gnou). Journal of Comparative Physiology A: Molecular habitat use by a small diurnal rodent (Octodon de- and Integrative Physiology 191:1055–1064. gus) in a semiarid environment: thermoregulatory Marai I. F. M., Haeeb A. A. M. 2010. Buffalo’s biolog- constraints or predation risk? Journal of Mammalogy ical functions as affected by heat stress—a review. 76:900–905. Livestock Science 127:89–109. Langman V. A., Maloiy G. M. O., Schmidt-Nielsen K., Mares M. A. 1977a. Water economy and salt balance Schroter R. C. 1979. Nasal heat exchange in the in a South American desert rodent, Eligmodontia giraffe and other large mammals. Respiration Phys- typus. Comparative Biochemistry and Physiology Part A: iology 37:325–333. Physiology 56:325–332.

Mares M. A. 1977b. Water independence in a South Nagy K. A. 1994. Seasonal water, energy and food use American non-desert rodent. Journal of Mammalogy by free-living, arid-habitat mammals. Australian 58:653–656. Journal of Zoology 42:55–63. Mares M. A. 1993. Desert rodents, seed consumption, Nagy K. A., Knight M. H. 1994. Energy, water, and food use and convergence: evolutionary shuffling of adap- by springbok antelope (Antidorcas marsupialis) in the tations. BioScience 43:372–379. Kalahari desert. Journal of Mammalogy 75:860–872. Marsh A. C., Louw G., Berry H. H. 1978. Aspects of Naya D. E., Bacigalupe L. D., Bustamante D. M., Boz- renal physiology, nutrition and therrnoregula- inovic F. 2005. Dynamic digestive responses to in- tion in the ground squirrel Xerus inauris. Madoqua creased energy demands in the leaf-eared mouse 2:129–135. (Phyllotis darwini). Journal of Comparative Physiology Mbassa G. K. 1988. Mammalian renal modifications B: Biochemical, Systems, and Environmental Physiology in dry environments. Veterinary Research Communi- 175:31–36. cations 12:1–18. Nel J. A. J. 1984. Behavioural ecology of canids in McCutchen H. E. 1981. Desert bighorn zoogeography the south-western Kalahari. Koedoe Supplement and adaptation in relation to historic land use. (1984):229–235. Wildlife Society Bulletin 9:171–179. Noll-Banholzer U. 1979. Body temperature, oxygen McKean T., Walker B. 1974. Comparison of selected consumption, evaporative water loss and heart cardiopulmonary parameters between the prong- rate in the fennec. Comparative Biochemistry and horn and the goat. Respiration Physiology 21:365– Physiology Part A: Physiology 62:585–592. 370. Nowack J., Dausmann K. H., Mzilikazi N. 2013. Non- Mendelssohn H., Yom-Tov Y. 1999. Mammalia of Israel. shivering thermogenesis in the African lesser Jerusalem (Israel): Israel Academy of Sciences and bushbaby, Galago moholi. Journal of Experimental Bi- Humanities. ology 216:3811–3817. Mengistu U., Dahlborn K., Olsson K. 2007. Effects of Osborn S. D. 1991. Adaptive heterothermy in desert intermittent watering on water balance and feed mammals. [PhD thesis]. Tucson (Arizona): Uni- intake in male Ethiopian Somali goats. Small Rumi- versity of Arizona. nant Research 67:45–54. Ostrowski S., Williams J. B. 2006. Heterothermy of Merkt J. R., Taylor C. R. 1994. “Metabolic switch” for free-living Arabian sand gazelles (Gazella subgut- desert survival. Proceedings of the National Academy turosa marica) in a desert environment. Journal of of Sciences of the United States of America 91:12313– Experimental Biology 209:1421–1429. 12316. Ostrowski S., Williams J. B., Bedin E., Ismail K. 2002. Misra A. K., Singh K. 2002. Effect of water deprivation Water influx and food consumption of free-living on dry matter intake, nutrient utilization and met- oryxes (Oryx leucoryx) in the Arabian desert in abolic water production in goats under semi-arid summer. Journal of Mammalogy 83:665–673. zone of India. Small Ruminant Research 46:159–165. Ostrowski S., Williams J. B., Ismael K. 2003. Hetero- Mitchell D., Maloney S. K., Laburn H. P., Knight thermy and the water economy of free-living Ara- M. H., Kuhnen G., Jessen C. 1997. Activity, blood bian oryx (Oryx leucoryx). Journal of Experimental temperature and brain temperature of free- Biology 206:1471–1478. ranging springbok. Journal of Comparative Physiology Ostrowski S., Williams J. B., Mésochina P., Sauerwein B: Biochemical, Systems, and Environmental Physiology H. 2006. Physiological acclimation of a desert an- 167:335–343. telope, Arabian oryx (Oryx leucoryx), to long-term Mitchell D., Maloney S. K., Jessen C., Laburn H. P., food and water restriction. Journal of Comparative Kamerman P. R., Mitchell G., Fuller A. 2002. Adap- Physiology B: Biochemical, Systems, and Environmental tive heterothermy and selective brain cooling Physiology 176:191–201. in arid-zone mammals. Comparative Biochemistry Ouajd S., Kamel B. 2009. Physiological particularities and Physiology B: Biochemistry and Molecular Biology of dromedary (Camelus dromedarius) and experi- 131:571–585. mental implications. Scandinavian Journal of Labo- Mitchell J., Mitchell G., Lust A. 2009. Thermoregu- ratory Animal Science 36:19–29. latory anatomy of pronghorn (Antilocapra ameri- Oyewale J., Dzenda T., Yaqub L., Akanbi D., Ayo J., cana). European Journal of Wildlife Research 55:23–31. Owoyele O., Minka N., Dare T. 2011. Alterations Morton S. R. 1978. An ecological study of Sminthop- in the osmotic fragility of camel and donkey eryth- sis carasicaudata (Marsupialia: Dasyuridae). III. rocytes caused by temperature, pH and blood stor- Reproduction and life history. Australian Wildlife age. Veterinarski Arhiv 81:459–470. Research 5:183–211. Peinke D. M., Brown C. R. 1999. Osmoregulation and Murray B. R., Dickman C. R., Watts C. H. S., Morton water balance in the springhare (Pedetes capensis). S. R. 1999. The dietary ecology of Australian ro- Journal of Comparative Physiology B: Biochemical, Sys- dents. Wildlife Research 26:857–858. tems, and Environmental Phsyiology 169:1–10.

Perrin M. R., Downs C. T. 1994. Comparative aspects Saadi L., Lebaili N. 2012. Effect of a water-rich diet of the thermal biology of the Cape spiny mouse, on adrenal zone glomerulosa in Gerbillus tarabuli. Acomys subspinosus, and the common spiny mouse, Comptes Rendus Biologies 335:96–102. A. spinosissimus. Israel Journal of Zoology 40:151–160. Salsamendi E., Arostegui I., Aihartza J., Almenar D., Portas T. J., Lynch M. J., Vogelnest L. 2003. Com- Goiti U., Garin I. 2012. Foraging ecology in Mehely’s parison of etorphine-detomidine and medetomi- horseshoe bats: influence of habitat structure and dine-ketamine anesthesia in captive addax (Addax water availability. Acta Chiropterologica 14:121–132. nasomaculatus). Journal of Zoo and Wildlife Medicine Sassi P. L., Borghi C. E., Bozinovic F. 2007. Spatial 34:269–273. and seasonal plasticity in digestive morphology Purohit K. G. 1971. Absolute duration of survival of of cavies (Microcavia australis) inhabiting habitats tammar wallaby (Macropus eugenii, Marsupialia) with different plant qualities. Journal of Mammalogy on sea water and dry food. Comparative Biochemistry 88:165–172. and Physiology Part A: Physiology 39:473–481. Sassi P. L., Caviedes-Vidal E., Anton R., Bozinovic F. Rainho A. 2007. Summer foraging habitats of bats in 2010. Plasticity in food assimilation, retention a Mediterranean region of the Iberian Peninsula. time and coprophagy allow herbivorous cavies Acta Chiropterologica 9:171–181. (Microcavia australis) to cope with low food quality Randall J. A. 1997. Species-specific footdrumming in in the Monte desert. Comparative Biochemistry and kangaroo rats: Dipodomys ingens, D. deserti, D. specta- Physiology Part A: Molecular and Integrative Physiology bilis. Animal Behaviour 54:1167–1175. 155:378–382. Randall J. A., Rogovin K., Parker P. G., Eimes J. A. Scantlebury M., Bennett N. C., Speakman J. R., Pillay 2005. Flexible social structure of a desert rodent, N., Schradin C. 2006. Huddling in groups leads Rhombomys opimus: philopatry, kinship, and ecolog- to daily energy savings in free-living African four- ical constraints. Behavioral Ecology 16:961–973. striped grass mice, Rhabdomys pumilio. Functional Rathbun G. B., Rathbun C. D. 2005. Noki or dassie- Ecology 20:166–173. rat (Petromus typicus) feeding ecology and petro Schmid J. 2001. Daily torpor in free-ranging gray phily. Belgian Journal of Zoology 135(Supplement): mouse lemurs (Microcebus murinus) in Madagascar. 69–75. International Journal of Primatology 22:1021–1031. Rautenstrauch K. R., Krausman P. R. 1989. Influence Schmid J., Speakman J. R. 2009. Torpor and energetic of water availability and rainfall on movements of consequences in free-ranging grey mouse lemurs desert mule deer. Journal of Mammalogy 70:197–201. (Microcebus murinus): a comparison of dry and wet Reese J. B., Haines H. 1978. Effects of dehydration on forests. Naturwissenschaften 96:609–620. metabolic rate and fluid distribution in the jack- Schmidt-Nielsen B., Schmidt-Nielsen K. 1951. A com- rabbit, Lepus californicus. Physiological Zoology 51: plete account of the water metabolism in kanga- 155–165. roo rats and an experimental verification. Journal Rickart E. A. 1986. Serum thyroxine and seasonal fat- of Cellular and Comparative Physiology 38:165–181. tening of free-living piute ground squirrels, Sper- Schmidt-Nielsen B., Schmidt-Nielsen K., Houpt T. R., mophilus mollis (Rodentia: Sciuridae). Comparative Jarnum S. A. 1956. Water balance of the camel. Biochemistry and Physiology Part A: Physiology 85: American Journal of Physiology 185:185–194. 199–202. Schmidt-Nielsen K., Schmidt-Nielsen B. 1952. Water Ron U., Haim A. 2001. How dehydration affects the metabolism of desert mammals. Physiological Re- thermoregulatory and osmoregulatory abilities of views 32:135–166. the golden spiny mouse Acomys russatus. Israel Jour- Schmidt-Nielsen K., Schmidt-Nielsen B., Brokaw A. nal of Zoology 47:15–20. 1948. Urea excretion in desert rodents exposed to Rubal A., Choshniak I., Haim A. 1992. Daily rhythms high protein diets. Journal of Cellular and Compara- of metabolic rate and body temperature of two tive Physiology 32:361–379. murids from extremely different habitats. Chrono- Schmidt-Nielsen K., Crawford E. C. Jr., Newsome A. E., biology International 9:341–349. Rawson K. S., Hammel H. T. 1967. Metabolic rate Rübsamen K., Kettembeil S. 1980. Effect of water re- of camels: effect of body temperature and dehy- striction on oxygen uptake, evaporative water loss dration. American Journal of Physiology 212:341–346. and body temperature of the rock hyrax. Journal Schmidt-Nielsen K., Hainsworth F. R., Murrish D. E. of Comparative Physiology B: Biochemical, Systems, and 1970. Counter-current heat exchange in the respi- Environmental Physiology 138:315–320. ratory passages: effect on water and heat balance. Rugangazi B. M., Maloiy G. M. O. 1988. Renal excre- Respiration Physiology 9:263–276. tion of urea in a small east African antelope, the Schmidt-Nielsen K., Schroter R. C., Shkolnik A. 1981a. dik-dik (Rhynchotragus kirkii). Comparative Biochem- Desaturation of exhaled air in camels. Proceedings istry and Physiology Part A: Physiology 91:437–444. of the Royal Society B: Biological Sciences 211:305–319.

Schmidt-Nielsen K., Crawford E. C., Hammel H. T. Schulz E., Fraas S., Kaier T. M., Cunningham P. L., 1981b. Respiratory water loss in camels. Proceedings Ismail K., Wronski T. 2013. Food preferences and of the Royal Society B: Biological Sciences 211:291–303. tooth wear in the sand gazelle (Gazella marica). Schoepf I., Schradin C. 2014. Arginine vasopressin Mammalian Biology 78:55–62. plasma levels change seasonally in African striped Schumann D. M., Cooper H. M., Hofmeyr M. D., Ben- mice but do not differ between alternative repro- nett N. C. 2005. Circadian rhythm of locomotor ductive tactics. General and Comparative Endocrinol- activity in the four-striped field mouse, Rhabdomys ogy 204:43–48. pumilio: a diurnal African rodent. Physiology and Be- Schradin C. 2005. Nest-site competition in two diurnal havior 85:231–239. rodents from the succulent karoo of South Africa. Selim H. M., Imai S., El Sheik A. K., Attia H., Oka- Journal of Mammalogy 86:757–762. moto E., Miyagawa E., Maede Y. 1999. Rumen cili- Schradin C. 2006. Whole-day follows of striped mice ate protozoal fauna of native sheep, friesian cattle (Rhabdomys pumilio), a diurnal murid rodent. Jour- and dromedary camel in Libya. Journal of Veterinary nal of Ethology 24:37–43. Medical Science 61:303–305. Schradin C., Pillay N. 2005a. Demography of the Shanas U., Haim A. 2004. Diet salinity and vasopressin striped mouse (Rhabdomys pumilio) in the succu- as reproduction modulators in the desert-dwelling lent karoo. Mammalian Biology 70:84 –92. golden spiny mouse (Acomys russatus). Physiology Schradin C., Pillay N. 2005b. Intraspecific variation and Behavior 81:645–650. in the spatial and social organization of the Af- Shaw W. T. 1934. The ability of the giant kangaroo rat rican striped mouse. Journal of Mammalogy 86: as a harvester and storer of seeds. Journal of Mam- 99–107. malogy 15:275–286. Schradin C., Pillay N. 2006. Female striped mice Shkolnik A., Borut A. 1969. Temperature and water (Rhabdomys pumilio) change their home ranges in relations in two species of spiny mice (Acomys). response to seasonal variation in food availability. Journal of Mammalogy 50:245–255. Behavioral Ecology 17:452–458. Shoemaker V. H., Nagy K. A., Costa W. R. 1976. Energy Schradin C., Krackow S., Schubert M., Keller C., utilization and temperature regulation by jack- Schradin B., Pillay N. 2007. Regulation of activity rabbits (Lepus californicus) in the Mojave Desert. in desert-living striped mice: the importance of Physiological Zoology 49:364 –375. basking. Ethology 113:606–614. Siebert B. D., Macfarlane W. V. 1971. Water turnover Schradin C., Schmohl G., Rödel H. G., Schoepf I., and renal function of dromedaries in the desert. Treffler S. M., Brenner J., Bleeker M., Schubert M., Physiological Zoology 44:225–240. König B., Pillay N. 2010. Female home range size Siebert B. D., Macfarlane W. V. 1975. Dehydration in des- is regulated by resource distribution and intraspe- ert cattle and camels. Physiological Zoology 48:36–48. cific competition: a long-term field study. Animal Silanikove N., Tagari H., Shkolnik A. 1980. Gross en- Behaviour 79:195–203. ergy digestion and urea recycling in the desert Schradin C., Lindholm A. K., Johannesen J., Scho- black Bedouin goat. Comparative Biochemistry and epf I., Yuen C.-H., König B., Pillay N. 2012. Social Physiology Part A: Physiology 67:215–218. flexibility and social evolution in mammals: a case Sneddon J. C., Boomker E., Howard C. V. 2006. Mucosal study of the African striped mouse (Rhabdomys surface area and fermentation activity in the hind pumilio). Molecular Ecology 21:541–553. gut of hydrated and chronically dehydrated work- Schradin C., Raynaud J., Arrivé M., Blanc S. 2014. ing donkeys. Journal of Animal Science 84:119–124. Leptin levels in free ranging striped mice (Rhab- Soholt L. F. 1974. Environmental conditions in an artifi- domys pumilio) increase when food decreases: the cial burrow occupied by Merriam’s kangaroo rat, Di- ecological leptin hypothesis. General and Compara- podomys merriami. Journal of Mammalogy 55:859–864. tive Endocrinology 206:139–145. Song X., Geiser F. 1997. Daily torpor and energy ex- Schreiber R. K. 1979. Coefficients of digestibility and penditure in Sminthopsis macroura: interactions be- caloric diet of rodents in the northern Great Basin tween food and water availability and temperature. desert. Journal of Mammalogy 60:416–420. Physiological Zoology 70:331–337. Schreier A. L., Swedell L. 2012. Ecology and sociality Spalton J. A. 1999. The food supply of the Arabian in a multilevel society: ecological determinants oryx (Oryx leucoryx) in the desert of Oman. Journal of spatial cohesion in Hamadryas baboons. Amer- of Zoology 248:433–441. ican Journal of Physical Anthropology 148:580–588. Stewart D. R. M. 1963. The Arabian oryx (Oryx leucoryx Schubert M., Pillay N., Ribble D. O., Schradin C. 2009. Pallas). African Journal of Ecology 1:103–117. The round-eared sengi and the evolution of social Taylor C. R. 1969. Metabolism, respiratory changes, monogamy: factors that constrain males to live and water balance of an antelope, the eland. Amer- with a single female. Ethology 115:972–985. ican Journal of Physiology 217:317–320.

Taylor C. R. 1970a. Dehydration and heat: effects on Williams J. B., Lenain D., Ostrowski S., Tielman B. I., temperature regulation of East African ungulates. Seddon P. J. 2002. Energy expenditure and water American Journal of Physiology 219:1136–1139. flux of Rüppell’s foxes in Saudi Arabia. Physiologi- Taylor C. R. 1970b. Strategies of temperature regula- cal and Biochemical Zoology 75:479–488. tion: effect on evaporation in East African ungu- Wilson R. T. 1989. Ecophysiology of the Camelidae and Des- lates. American Journal of Physiology 219:1131–1135. ert Ruminants. Berlin (Germany): Springer-Verlag. Timm R. M., Kermott L. H. 1982. Subcutaneous and Winkelmann J. R., Getz L. L. 1962. Water balance in the cutaneous melanins in Rhabdomys: complementary Mongolian gerbil. Journal of Mammalogy 43:150–154. ultraviolet radiation shields. Journal of Mammalogy Withers P. C., Cooper C. E. 2009. Thermal, metabolic, and 63:16–22. hygric physiology of the little red kaluta, Dasykaluta Tirado C., Cortés A., Bozinovic F. 2008. Water balance rosamondae (Dasyuromorphia: Dasyuridae). Journal of in two South American Phyllotis desert rodents, P. Mammalogy 90:752–760. xanthopygus rupestris and P. darwini darwini. Journal Withers P. C., Lee A. K., Martin R. W. 1979. Metabolism, of Arid Environments 72:664–670. respiration and evaporative water loss in the Aus- Turner J. C. 1970. Water consumption of desert big- tralian hopping-mouse Notomys alexis (Rodentia: horn sheep. Desert Bighorn Council Transactions Muridae). Australian Journal of Zoology 27:195–204. 14:189–197. Wittenberg C., Choshniak I., Shkolnik A., Thurau K., Turner J. C. 1979. Osmotic fragility of desert bighorn Rosenfeld J. 1986. Effect of dehydration and rapid sheep red blood cells. Comparative Biochemistry and rehydration on renal function and on plasma re- Physiology Part A: Physiology 64:167–175. nin and aldosterone levels in the black Bedouin Veloso C., Bozinovic F. 1993. Dietary and digestive goat. Pflügers Archiv 406:405–408. constraints on basal energy metabolism in a small Woodroffe R. 2011. Ranging behaviour of African herbivorous rodent. Ecology 74:2003–2010. wild dog packs in a human-dominated landscape. Vermeulen H. C., Nel J. A. J. 1988. The bush Karoo rat Journal of Zoology 283:88–97. Otomys unisulcatus on the Cape West coast. South Yagil R. 1985. The desert camel: comparative physi- African Journal of Zoology 23:103–111. ological adaptation. Comparative Animal Nutrition Walker F. M., Taylor A. C., Sunnucks P. 2007. Does soil 5:1–164. type drive social organization in southern hairy- Young R. A. 1976. Fat, energy and mammalian sur- nosed wombats? Molecular Ecology 16:199–208. vival. American Zoologist 16:699–710. Walsberg G. E. 1988. Consequences of skin color and Yousef M. K., Johnson H. D. 1975. Thyroid activity in fur properties for solar heat gain and ultraviolet desert rodents: a mechanism for lowered metabolic irradiance in two mammals. Journal of Comparative rate. American Journal of Physiology 229:427–431. Physiology B: Biochemical, Systems, and Environmental Yousef M. K., Dill D. B., Mayes M. G. 1970. Shifts in Physiology 158:213–221. body fluids during dehydration in the burro, Equus Warneke L., Turner J. M., Geiser F. 2008. Torpor and asinus. Journal of Applied Physiology 29:345–349. basking in a small arid zone marsupial. Naturwis- Zervanos S. M., Hadley N. F. 1973. Adaptational biology senschaften 95:73–78. and energy relationships of the collared peccary (Ta- Waterman J. M., Herron M. D. 2004. Xerus princeps. yassu tajacu). Ecology 54:759–774. Mammalian Species 751:1–3. Zhang Z.-Q., Wang D.-H. 2007. Seasonal changes in ther- Williams J. B., Ostrowski S., Bedin E., Ismail K. 2001. mogenesis and body mass in wild Mongolian gerbils Seasonal variation in energy expenditure, water flux (Meriones unguiculatus). Comparative Biochemistry and food consumption of Arabian oryx Oryx leuco- and Physiology Part A: Molecular and Integrative ryx. Journal of Experimental Biology 204:2301–2311. Physiology 148:346–353.

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