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Direct impacts of climatic warming on heat stress in endothermic species: seabirds as bioindicators of changing thermoregulatory constraints

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There is now abundant evidence that contemporary climatic change has indirectly affected a wide-range of species by changing trophic interactions, competition, epidemiology and habitat. However, direct physiological impacts of changing climates are
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  © 2012 ISZS, Blackwell Publishing and IOZ/CAS 121 123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051 Direct impacts of climatic warming on heat stress in endothermic species: seabirds as bioindicators of changing thermoregulatory constraints Stephen A. OSWALD and Jennifer M. ARNOLD Division of Science, Pennsylvania State University, Berks Campus, Reading, Pennsylvania, USA Abstract There is now abundant evidence that contemporary climatic change has indirectly affected a wide-range of spe-cies by changing trophic interactions, competition, epidemiology and habitat. However, direct physiological im- pacts of changing climates are rarely reported for endothermic species, despite being commonly reported for ec-totherms. We review the evidence for changing physiological constraints on endothermic vertebrates at high temperatures, integrating theoretical and empirical perspectives on the morphology, physiology and behavior of marine birds. Potential for increasing heat stress exposure depends on changes in multiple environmental vari- ables, not just air temperature, as well as organism-specic morphology, physiology and behavior. Endotherms  breeding at high latitudes are vulnerable to the forecast, extensive temperature changes because of the adap-tations they possess to minimize heat loss. Low-latitude species will also be challenged as they currently live close to their thermal limits and will likely suffer future water shortages. Small, highly-active species, particu-larly aerial foragers, are acutely vulnerable as they are least able to dissipate heat at high temperatures. Overall, direct physiological impacts of climatic change appear underrepresented in the published literature, but avail-able data suggest they have much potential to shape behavior, morphology and distribution of endothermic spe-cies. Coincidence between future heat stress events and other energetic constraints on endotherms remains largely unexplored but will be key in determining the physiological impacts of climatic change. Multi-scale,  biophysical modeling, informed by experiments that quantify thermoregulatory responses of endotherms to heat stress, is an essential precursor to urgently-needed analyses at the population or species level. Key words: climatic change, direct effects of climate, physiology, seabirds, thermoregulation  Integrative Zoology  2012; 7: 121–136doi: 10.1111/j.1749-4877.2012.00287.x REVIEW Correspondence : Stephen A. Oswald, Pennsylvania State University, Berks Campus, PO Box 7009, Tulpehocken Road, Reading, Pennsylvania 19610, USA. Email: steve.oswald@psu.edu INTRODUCTION Changing air temperatures at the ocean and land sur-face rank as the most dominant consequence of recent climatic change (Trenberth et al. 2007) and the main factor driving biotic responses (Parmesan & Yohe 2003; Walther   et al.  2005; Hansen et al.  2006; Pörtner & Far-rell 2008). Responses are observable across taxa and in-  © 2012 ISZS, Blackwell Publishing and IOZ/CAS 122 123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051 S. A. Oswald and J. M. Arnold clude changes in phenology (timing of activities), de-mography (population processes), distribution (species ranges) and individual behavior (Walther et al.  2002; Parmesan 2006). Impacts of climatic change can be  broadly categorized into either direct physiological ef-fects (e.g. thermoregulation) or indirect biotically-medi-ated effects (e.g. competition and resource availability). For vertebrates, more studies have addressed the direct thermoregulatory consequences of climatic change for ectotherms than for endotherms, presumably because ectothermic organisms rely more heavily on exogenous heat exchange for thermal homeostasis. Direct effects of climate change on ectotherms include adverse and bene- cial consequences for development (more rapid devel -opment of insect larvae and skewed reptile sex ratios), reproductive capacity (increased insect egg production and reduced hatching success of amphibian eggs), dis- persal (more highly dispersive insect phenotypes) and survival (reduced overwinter mortality for insects) (Gib- bon et al.  2000; Thomas et al. 2001; Bale et al. 2002; Walther et al. 2002;   Davies et al.  2006;   Hawkes et al.  2007). Despite regional variation (Christensen et al.  2007), surface temperatures are generally increasing as a result of contemporary climatic change (IPCC 2007; Trenberth et al  . 2007), challenging the thermoregulatory abilities of both ectotherms and endotherms at their upper ther-mal limits (Pörtner & Farrell 2008; Boyles et al. 2011). Although thermogenesis increases the capacity of endo-therms to maintain thermal homeostasis under challeng-ing environmental conditions, it comes at an energet-ic cost and inhibits activity at the 2 extremes of thermal stress (McNab 2002). Therefore, despite being more able to buffer challenging thermal environments, lim-its exist where thermoregulatory demands must con-strain the behavior of endotherms. These limits can be formalized by performance curves (Fig. 1) that describe the thermal optima for specic activities (from behavior to enzyme function) and the thermal range over which a certain level of activity can be maintained (performance  breadth) (Angilletta et al. 2010; Boyles et al. 2011). Be-cause there are limits to thermal adaptation and pheno-typic variability, thermal sensitivities of a wide range of physiological processes must logically provide abso-lute bounds on the populations and ranges of endother-mic species (Angilletta et al. 2010; Boyles et al. 2011). Consequently, direct thermoregulatory impacts of rap-idly changing climates should logically be expected for endothermic organisms as well as ectotherms, particu-larly at upper thermal limits (Fig. 1; Fuller et al. 2010; Boyles et al. 2011). Rising maximum environmental temperatures might impose direct and immediate physiological constraints upon endothermic species: theoretically, much more rap-idly than lagged indirect climatic effects through biotic interactions. To date, most studies of endothermic species have focused on indirect effects of climate as the drivers of distribution, population and behavioral-level chang-es (Crick 2004; Berteaux et al.  2006). Among these, the most pervasive drivers are changes in the timing, avail-ability and quality of food (e.g. Croxall et al.  2002); changes in biotic interactions (competition, predation and epidemiology) (e.g. Tylianakis et al.  2008); and changes in habitat availability and quality (e.g. Grego-ry et al.  2009). Except as cues for migration or hiber  -nation (e.g. Inouye et al. 2000),   direct thermal impacts of climatic change are rarely described for endothermic taxa (despite logical energetic constraints imposed by climate) and have only recently received attention as an important research area (Kearney & Porter 2009; Por-ter & Kearney 2009; Boyles et al.  2011; Oswald et al.  2011). Our purpose is to address this by reviewing the differential capacity of endotherms to accommodate cli-mate-induced heat stress given differences in morpholo-gy, physiology and behavior.We discuss behavioral and physiological mecha-nisms that endotherms use to thermoregulate (dissi- pate excess heat) at their upper thermal limits. Although heat loss can be detrimental at low temperatures, our fo-cus is on animals’ upper thermal limits so we consider Figure 1  Hypothetical performance curve illustrating limits of endotherm performance in relation to environmental temper-ature. Thermal optimum (T opt ), performance breadth (P  breadth ), critical thermal limits (CT min  and CT max ), and maximal perfor-mance (P max ) are shown (reproduced from Boyles et al.  2011). [P max ][T opt ]CT min      P    e    r     f    o    r    m    a    n    c    e Body temperatureCT max P  breadth  © 2012 ISZS, Blackwell Publishing and IOZ/CAS 123 123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051 Thermal demands of climate on endotherms heat loss or dissipation to be advantageous. Capacity to cope with changing thermoregulatory demands will de- pend on flexibility in morphology, physiology and be-havior (thermal adaptation) both via microevolutionary change (Angilletta et al.  2010) and as a result of pheno-typic plasticity (Fuller et al.  2010; Boyles et al.  2011). For species where thermoregulatory capacity is exceed-ed, range shifts or extinction will result (Thomas et al.  2004; Fuller et al.  2010). It is possible that chang- ing thermoregulatory regimes may be insufcient to in -duce changes in distribution or persistence (at least ini-tially) and, in these cases, consequences are complex  but can be generalized to compensative changes in ener-gy expenditure, time budgets and mortality risk (Angil-letta 2009). In the majority of cases, energy or time pre-viously invested in growth or reproduction would have to be used for active thermoregulation (e.g. panting and avoidance behaviors; McNab 2002). Alternatively, where no adjustment or increased energy expenditure is  possible, individuals might suffer increased risk of death (Angilletta 2009). Using seabirds as models for endotherms, we review the evidence for these responses and constraints from  physiology-based studies at the individual and regional scale. We identify important but generally neglected re-search areas and the most promising methodological ap- proaches for future studies. COLONIAL SEABIRDS AS BIOINDICATORS OF THERMOREGULATORY CHANGE We define a seabird as any species of the orders Sphenisciformes, Procellariiformes, and Pelecaniformes (excluding anhingas); and skuas, gulls, terns, skimmers and auks from the order Charadriiformes (Schreiber & Burger 2002). We suggest that, of these species, those likely to best serve as bioindicators of changing ther-moregulatory regimes have the following characteris-tics: (i) medium-distance or long-distance migrations; (ii) thermally-exposed breeding sites; (iii) strong depen-dence on marine prey; and (iv) well documented ther-moregulatory adaptations and behaviors.Although studying the thermoregulatory regimes of migrants that travel hundreds to thousands of miles be-tween breeding and wintering habitat might seem to in-crease the complexity of determining direct climat-ic constraints, there are certain conditions under which this greatly simplies the task. The unequal constraints on thermoregulatory behaviors should logically make  breeding sites more thermally stressful. Breeding uti-lizes a considerable proportion of a bird’s time and en-ergy budget (Ricklefs 1983; McNab 2002), constrains  birds to nesting sites often fully exposed to the elements and demands that seabirds act as central place foragers,  breeding on land and feeding at sea (Bried & Jouventin 2002). Therefore, it seems more likely that heat loss ca- pacity has evolved in response to conditions at breeding grounds for these migratory species rather than at winter roosts where individuals are free to engage in any ther-moregulatory activity, are less energetically constrained  by the demands of reproduction and can roam widely in search of food (e.g. BirdLife International 2004). Most seabird species have little opportunity to avoid incident solar radiation at breeding sites (often charac-terized by low lying vegetation) or while foraging at sea, leaving them exposed to extreme environmental heat gain. As such, ground-nesting or cliff-nesting spe-cies and those that nest on small shrubs or trees (where nests are not concealed within the foliage) are likely to  be far more sensitive bioindicators than burrow-nest-ing or cavity-nesting seabirds. Regular reports of ac-tive thermoregulation by breeding seabirds (e.g. Lustick 1984) provide circumstantial evidence of the potential for future constraint (under climatic warming scenarios) on breeding activity, possibly leading to reduced repro-ductive output (Oswald et al.  2008). Additionally, large-scale, multi-species studies report associations between  breeding distributions and heat stress conditions that are independent of foraging constraints (Nudds & Oswald 2007; Oswald et al.  2011).As many of these species depend largely on marine  prey, it is also possible to dissociate the confounding in-direct impacts of climate on prey availability and qual-ity (which occur at sea) from direct thermoregulato-ry constraints at breeding colonies (Oswald et al.  2011). Thus, for these species, responses to climatic conditions at breeding sites can be differentiated from responses to climatically-induced changes in prey availability or quality.Since the early 1950s, there have been many studies on the thermal relations and thermoregulatory mecha-nisms of seabirds (discussed below), and this has led to an understanding of thermoregulatory limitations that is  prerequisite for assessing vulnerability to the direct ef-fects of climatic warming. In the next section, we dis-cuss the environmental factors that cause heat stress for these endotherms and describe the various mechanisms that seabirds use to ameliorate this stress.  © 2012 ISZS, Blackwell Publishing and IOZ/CAS 124 123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051 S. A. Oswald and J. M. Arnold HEAT DISSIPATION AT THE INDIVIDUAL SCALE For endothermic organisms, the specic range of en -vironmental temperatures over which energy used for thermoregulation is relatively low (effectively at a bas-al level) is termed the thermal neutral zone (TNZ) (Ro-manovsky et al.  2002) (Fig. 2). Below lower critical temperatures (T lc ) and above upper critical temperatures (T uc ), the organism must expend more energy to main-tain thermal homeostasis (Fig. 2). Thus, changes in cli-matically-induced thermal stress upon endothermic spe-cies can be estimated from the length of exposure to environmental temperatures above the TNZ. Although these temperatures are commonly indexed by air tem-  perature (ambient temperature, Fig. 2), the specic ther  -mal loading on an organism results from both its thermal  properties and a number of climatic variables (Monteith & Unsworth 1990; McNab 2002). This can be formal-ized in a steady-state energy balance model (Fig. 3) that calculates the difference between energetic contribu-tions of thermal inputs and outputs (O’Conner & Spoti-la 1992). Such models have a long tradition in studies of ectotherms (as reviewed by O’Conner & Spotila 1992),  but are more rarely used for endothermic species (Conley & Porter 1986; Porter et al.  1994; Cartar & Morrison 1997; McCafferty et al.  2001; Porter & Kearney 2009). Although heat can be both lost and gained by all transfer processes (except metabolic heat production and short-wave [solar] radition), because our focus is active thermoregulation above the TNZ, we consider evapo-ration, convection and conduction as routes of heat dis-sipation rather than heat gain (Fig. 3). Because thermal exposure is not simply a matter of increasing air temper-ature, we now consider processes of heat gain (metabol-ic heat production and solar radiation) and heat loss (re-spiratory evaporation, convection, conduction and long-wave radiation) in turn. Metabolic heat generation In thermoregulating endotherms, the amount of heat  produced by metabolic activity (in addition to any ex-tra thermogensis from sources such as muscular exer-cise or digestion) must be equal to that lost to maintain core body temperature (Dawson & Whittow 2000). Al-though seabird core body temperatures generally range be-tween 36 and 40 °C at rest (Lustick 1984; Prinzinger et al.  1991), at high activity levels this can increase to 44 °C in some species (Prinzinger et al.  1991), and much of the variability in body temperature can be explained by size (McNab 1966) and ecology (Ellis 1984; Ellis & Gabri - elsen 2002). Thermogenesis in ight is much greater be -cause the metabolic rate generally increases between 2 and 11 times basal levels (Dawson 1975; Ellis 1984). Figure 2  Thermoregulation and the ther-mal neutral zone: schematic relation-ships among ambient temperature (T a ), metabolic heat production, heat loss and  body temperature (T  b ). T lc  = lower criti-cal temperature, T uc  = upper critical tem- perature (reproduced from Widowski 2010).  © 2012 ISZS, Blackwell Publishing and IOZ/CAS 125 123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051 Thermal demands of climate on endotherms Thus, small, highly-active species (e.g. flapping and  plunge-diving/pursuit-diving species [Ellis & Gabri -elsen 2002]) are likely to generate the highest metabolic heat burdens, particularly at high latitudes and for sea- birds that raise large broods and/or spend more time for- aging (Ellis & Gabrielsen 2002). Solar radiation Solar radiation (short-wave radiation Q s ; Fig. 3) can greatly increase heat loads on seabirds nesting in sparse vegetative cover and demand behavioral modications, such as orientation toward the sun and postural adjust-ments to minimize exposure of darker plumage surfaces (Lustick et al.  1978, 1980). Orientation to the sun might  be less important when the sun is directly overhead, such as later in the temperate breeding season or in the tropics (Lustick et al.  1978; Lustick 1984). Thus, the al-  bedo (reectance) of the bird, which can be altered by feather erection (Wolf & Walsberg 2000) and the inci-dence of sun exposure (Lustick et al.  1978) are both im- portant in determining heat loading from insolation (Fig. 3). There is considerable uncertainty surrounding future cloud cover scenarios (Christensen et al.  2007), but so-lar radiation will likely remain a major determinant of heat stress for seabirds breeding in largely unvegetated colonies, especially at lower latitudes (e.g. Hochscheid et al.  2002). Most seabird species have either light or dark color-ation or a mixture, and juveniles are often darker than adults. Dark plumages can result in increased rates of Figure 3  Components of heat stress: a generalized heat balance equation for endotherms, subtracting mechanisms of heat loss from mechanisms of heat gain. For each mechanism, its dependence on properties of the environment (grey text) and properties of the or- ganism (bold text) is formalized. (Equations are adapted from Monteith & Unsworth [1990], O’Conner & Spotila [1992] and Daw -son & Whittow [2000].) Metabolic heat production is largely proportional to body mass but exact relationships are species-depen- dent: metabolic rates during rest and/or activity can be estimated from body mass (e.g. Ellis & Gabrielsen [2002]; McKenchnie & Wolf [2004]).
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