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Abstract
Volume 11 • 2023 10.1093/conphys/coad011 Research article Riding out the storm: depleted fat stores and elevated hematocrit in a small bodied endotherm exposed to severe weather 1,2, 1,3 4 1 N.E. Freeman , M. Gustafson , T.J. Hee fl y and W.A. Boyle Division of Biology, Kansas State University, 116 Ackert Hall, Manhattan, KS 66506, USA School of Natural Sciences, Bangor University, Deiniol Road, Bangor, Gwynedd, LL57 2DG, UK Department of Biological Sciences, Boise State University, 2133 Cesar Chavez Lane, Boise, ID 83725, USA Department of Statistics, Kansas State University, 101 Dickens Hall, Manhattan, KS 66506, USA *Corresponding author: Division of Biology, Kansas State University, 116 Ackert Hall, Manhattan, KS 66506, USA. Email: koleyfree@gmail.com .......................................................................................................................................................... In the mid-continental grasslands of North America, climate change is increasing the intensity and frequency of extreme weather events. Increasingly severe storms and prolonged periods of elevated temperatures can impose challenges that adversely affect an individual’s condition and, ultimately, survival. However, despite mounting evidence that extreme weather events, such as heavy rain storms, can impose short-term physiological challenges, we know little regarding the putative costs of such weather events. To determine the consequences of extreme weather for small endotherms, we tested predictions of the relationships between both severe precipitation events and wet bulb temperatures (an index that combines temperature and humidity) prior to capture with body composition and hematocrit of grasshopper sparrows (Ammodramus savannarum) caught during the breeding season at the Konza Prairie Biological Station, Kansas, USA, between 2014 and 2016. We measured each individual’s fat mass, lean mass and total body water using quantitative magnetic resonance in addition to their hematocrit. Individuals exposed to storms in the 24 hours prior to capture had less fat reserves, more lean mass, more water and higher hematocrit than those exposed to moderate weather conditions. Furthermore, individuals stored more fat if they experienced high wet bulb temperatures in the week prior to capture. Overall, the analysis of these data indicate that extreme weather events take a physiological toll on small endotherms, and individuals may be forced to deplete fat stores and increase erythropoiesis to meet the physiological demands associated with surviving a storm. Elucidating the potential strategies used to cope with severe weather may enable us to understand the energetic consequences of increasingly severe weather in a changing world. Key words: QMR, precipitation, lean mass, fat stores, energetics, body composition Editor: Dr. Steven Cooke Received 5 August 2022; Revised 15 February 2023; Editorial Decision 21 February 2023; Accepted 14 March 2023 Cite as: Freeman NE, Gustafson M, Hefley TJ, Boyle WA (2023) Riding out the storm: depleted fat stores and elevated hematocrit in a small bodied endotherm exposed to severe weather. Conserv Physiol 11(1): coad011; doi:10.1093/conphys/coad011. .......................................................................................................................................................... .......................................................................................................................................................... © The Author(s) 2023. Published by Oxford University Press and the Society for Experimental Biology. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/ by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. Research article Conservation Physiology • Volume 11 2023 .......................................................................................................................................................... number of examples that link behaviour, physiology and Introduction demography to either too little or too much rain. Under Global variation in climate has had a profound influence on drought conditions, birds frequently experience lower repro- broad-scale patterns of species distribution via selection on ductive success (Skagen and Adams, 2012; Colón et al., traits that mediate organismal responses to weather (Pear- 2017), adjust movement (Bateman et al., 2015) or exhibit son and Dawson, 2003; Kearney and Porter, 2009). While altered abundance and patterns of occupancy (Albright et al., climates have changed over the evolutionary histories of all 2017; Cady et al., 2019). Responses to rainfall may reflect extant species, the current rates of change are unprecedented direct challenges to maintain internal homeostasis or may be (Alley et al., 2003; Smith et al., 2015). Consequently, species the result of indirect bottom-up (e.g. vegetation and habitat living in the modern world are coping with conditions that structure, prey communities) or top-down (e.g. predator com- may be at the limits of those under which they historically munities) processes (Boyle et al., 2020). Extreme precipitation thrived (O’Neill and Oppenheimer, 2004). The majority of events can also influence fitness directly. Storms are weather studies investigating species-level responses to changing cli- events lasting from hours to days with heavy rain, frequently mates have focused on rising temperatures and have doc- accompanied by high winds, lightning and thunder. During umented associated poleward range shifts (MacLean and and immediately following storms, some birds suffer nest Beissinger, 2017), shifts in phenology (Renner and Zohner, failure (Conrey et al., 2016), alter timing or investment in 2018; Piao et al., 2019) or changes in performance (Deutsch breeding activities (Mahony et al., 2006), move away from et al., 2008; Román-Palacios and Wiens, 2020). Importantly, affected regions (Ramos, 1989; Boyle et al., 2010), alter their climate change is far more complex than just increasing tem- physiology and body condition (Wingfield et al., 1998, 2017; peratures. As the world warms, precipitation regimes are also Krause et al., 2018) and sometimes, die (Newton, 2007; affected with some regions becoming drier and others becom- Wellicome et al., 2014). ing wetter (IPCC, 2022). Furthermore, altered patterns of While direct costs of rain on birds can be independent of temperature, humidity and rainfall are leading to widespread temperature, other potential costs result from interactions changes in the timing, severity and intervals between rain between temperature and humidity. At high temperatures, storms (IPCC, 2022). For example, mid-continental regions birds expend energy to maintain stable internal temperatures such as the Great Plains of North America are character- via evaporative cooling (Lasiewski et al., 1966; Pollock ized by substantial inter- and intra-annual variation in both et al., 2021). But, the effectiveness (i.e. energy cost) of temperature and precipitation (Cherwin and Knapp, 2012; evaporative cooling is dependent upon the strength of the Ojima et al., 2021). Projections for this region are for a mean moisture gradient between the air and mucous membranes ◦ ◦ temperature increase of 4.4 Cto6.6 C by 2099 and the such as the mouth or gular regions, where drier conditions number of days per year where temperatures exceed 32 Cis assist with evaporation (Lasiewski et al., 1966; van Dyk predicted to quadruple (Vose et al., 2017). Total precipitation et al., 2019). Therefore, under humid conditions, birds suffer is predicted to decline by 5% to 10% (Easterling et al., 2017), greater thermoregulatory costs and are at greater risk of fatal leading to more prolonged periods of drought but also higher- consequences of high temperatures (Gerson et al., 2014; intensity precipitation events (Janssen et al., 2014; Hicke McKechnie and Wolf, 2019). Thus, measures of environ- et al., 2022). mental conditions that take humidity into account, such as For endothermic animals such as birds, the effects of wet bulb temperature, are far more biologically relevant temperature on individual physiology, behaviour and survival to birds and have greater predictive power to explain are relatively well studied. Endotherms maintain stable core broad associations between climate and distributions than body temperatures and when ambient temperatures exceed the commonly used measure of temperature (i.e. dry bulb the upper and lower limits (i.e. upper and lower critical temperature; James, 1970). temperatures) of their thermoneutral zone, their metabolism Birds cope with severe weather variability by triggering increases (Scholander et al., 1950). A large suite of traits an ‘emergency life history stage’ (Wingfield et al., 1998; define the range of temperatures under which each species can Wingfield, 2013). When faced with challenges, vertebrates, maintain low energy expenditure including body size, con- including birds, activate hormonal pathways that result in ductance and metabolic rates (Mitchell et al., 2018; Gerson the release of a suite of hormones including catecholamines et al., 2019; McKechnie and Wolf, 2019). When faced with (e.g. epinephrine) and glucocorticoids into the bloodstream, elevated ambient temperatures that exceed the upper limit of which mobilize energy stores and influence body compo- their thermoneutral zone, endotherms can cope behaviourally sition (reviewed in Sapolsky et al., 2000; Wingfield et al., by seeking cooler microclimates (Etches et al., 2008), ceasing 2017). Fat is the component of body composition that pro- or reducing activities that generate excess body heat (Silva vides the greatest amount of energy per unit mass (Jenni et al., 2015) and actively cooling via evaporative water loss and Jenni-Eiermann, 1998), and in birds, can be rapidly (Lasiewski et al., 1966), leading to increased water intake to deposited and mobilized in response to short-term foraging battle dehydration (May and Lott, 1992). excesses or deficits (Dick et al., 2020). While fat deposi- Our understanding of how endotherms respond to precip- tion or mobilization can be regulated within minutes, body itation is substantially less complete, but there is a growing composition responses are typically evident within hours to .......................................................................................................................................................... 2 Conservation Physiology • Volume 11 2023 Research article .......................................................................................................................................................... days (Seewagen and Guglielmo, 2010; Boyle et al., 2012; increase to meet increased energy expenditure (Fair et al., Krause et al., 2017). Birds can also facultatively modulate 2007). Depending if temperatures are within a tolerable components of lean mass (i.e. muscles and organs; (Guglielmo range, fat or lean mass may remain constant or even increase. and Williams, 2003; Gerson and Guglielmo, 2011a), but gram However, if temperatures exceed the thermoneutral zone, we for gram, mobilization of lean mass yields less energy than predicted that individuals would then have lower fat and fat. Carbohydrates, fat and protein can be used to increase lean mass because energy would be required to maintain the fat stores, while lean mass growth requires a protein rich diet higher metabolic demand associated with thermoregulation. (Guglielmo et al., 2022), and thus, lean mass may respond Declines in fat and lean mass could also allow individuals to to environmental stressors more slowly than fat mass due cope with heat stress by lowering their metabolic heat load to the need of a more protein-rich diet. Depleted lean mass (Klaassen et al., 1990). Body water and hematocrit responses typically represents either a weight-saving strategy or a source also provide insight into whether individuals are capable of of metabolic water during flight, or more severe energy maintaining key elements of homeostasis or not under current depletion under starvation conditions (Karasov and Pinshow, weather conditions. Under hot conditions, which can lead to 1998; Gerson and Guglielmo, 2011b). dehydration via evaporative water loss, we expected body water to decrease and hematocrit to increase. Changes in weather may also impact an individual’s ability to maintain water homeostasis and, as a result, hematocrit. Water does not provide metabolic energy but is required for Methods functions from molecular to organ level scales (Gerson and Study site and species Guglielmo, 2011a). Animals may experience extreme dehy- dration leading to the shutdown of metabolic pathways and We conducted our study at the Konza Prairie Biological organs, and ultimately, death (e.g. Albright et al., 2017). Ele- ◦ ◦ Station (hereafter ‘Konza Prairie’, 39 05 N, 96 35 W) in vated temperatures may lead to dehydration resulting in more northeastern Kansas, USA. Konza Prairie is a native tallgrass concentrated blood (i.e. higher hematocrit; Fair et al., 2007). prairie composed of experimentally manipulated watersheds To combat dehydration, birds may drink or consume foods with replicated combinations of grazing (ungrazed or grazed rich in water (Bartholomew and Cade, 1963). Thus, rainfall by bison or cattle) and burning frequency (1-, 2-, 3-, 4-, may allow individuals to maintain water balance. Alterna- or 20-year intervals) treatments. The weather at Konza tively, individuals may endogenously produce water through Prairie is highly dynamic with a mean annual temperature of the catabolism of fat (Rutkowska et al., 2016) and protein 12 C and a mean annual precipitation of 835 mm (Goodin (Jenni and Jenni-Eiermann, 1998; Gerson and Guglielmo, et al., 2003). Precipitation varies considerably inter- and intra- 2011a). Maintenance of water balance allows for viscosity annually with the majority of rainfall occurring in May, June of blood to be maintained ensuring proper circulation and and September (Goodin et al., 2003). the oxygen transport. Understanding the interplay between We captured grasshopper sparrows at Konza Prairie water balance and blood is important because elevated hema- throughout their breeding season (April–August). Grasshop- tocrit is associated with migratory behaviour (Krause et al., per sparrows are small songbirds that breed in the grasslands 2016a) and energy expenditure (Yap et al., 2019) and has of North America, occupying in patchy grasslands with downstream consequences on survival (Bowers et al., 2014) few shrubs (Powell, 2008; Vickery, 2020). Throughout the including during winter and extreme weather (Fair et al., breeding season, individuals devote energy to finding mates, 2007; Krause et al., 2016b). building nests, incubating eggs (female only) and feeding young in addition to avoiding predators and surviving We quantified body composition and hematocrit of adult inclement weather (Vickery, 2020). Breeding pairs may grasshopper sparrows (Ammodramus savannarum) during attempt raising one to three broods per season due to high three breeding seasons at the Konza Prairie Biological Station rates of nest failure (Vickery, 2020). Furthermore, individuals in Kansas, USA. The grasshopper sparrow is a small, ground- may disperse within the breeding season. For example, 75% nesting passerine whose survival and abundance appear to of male grasshopper sparrows changed territories, moving up be strongly influenced by weather on both breeding and to 8.9 km (Williams and Boyle, 2018). non-breeding areas (Gorzo et al., 2016, Macías-Duarte et al., 2017, Silber et al., 2023). Thus, in order to survive All work was conducted under approved ethical animal rainstorms and periods of hot, humid weather, we expected care and use protocols (Kansas State University #3260) and birds to therefore modulate body composition and hematocrit research permits from the North American Bird Banding to meet the energetic demands of inclement weather. Storms Laboratory (#23836), Konza Prairie Biological Station and introduce foraging uncertainty that can lead to short-term the Kansas Department of Wildlife, Parks and Tourism. fasting, so we predicted that individuals would deplete fat and protein and therefore have lower fat and lean mass following Field methods a storm. Alternatively, rain may allow for rehydration, in which case total body water and therefore, lean mass would Throughout the breeding seasons of 2014–16, we caught increase. Following storms, we also expected hematocrit to adult grasshopper sparrows using mist nets. We marked birds .......................................................................................................................................................... 3 Research article Conservation Physiology • Volume 11 2023 .......................................................................................................................................................... using a unique combination of three coloured leg bands and wet bulb temperature explains size variation in birds better one US Fish and Wildlife Services issued aluminium, num- than air temperature (James, 1970). To assess the relationship bered leg band. Individuals were sexed based on the presence between body composition and weather in the week leading of a cloacal protuberance (male) or a brood patch (female) up to capture, we calculated the average wet bulb temperature and were weighed. Using a mobile quantitative magnetic in the 168 hours (= 1 week) prior to the capture time of each resonance (QMR) machine (Echo-Medical Systems, Houston, individual. We measured the average wet bulb temperature TX, USA), we estimated body composition of the individual across a weeklong period because we were interested in the (n = 325) by measuring fat mass (g), total body water (g) and cumulative effects of many hot, humid days in a row. lean mass (g) prior to release. Fat mass reflects the amount To assess the relationship between storms, body compo- of fat the bird has stored in addition to lipids in cellular sition and hematocrit, we first characterized precipitation membranes. Total body water is an estimate of the mass events. The start of a precipitation event was the first of the of all water in the tissues, including blood and any water 15-minute periods where rainfall was detected and contin- in the digestive and urinary systems. Lean mass estimates ued through all periods recording measurable precipitation. the mass of organs and tissues but also includes water (also Events ended at the time when no rain was detected in eight known as wet lean mass, Boyle et al., 2012). QMR has consecutive 15-minute periods (i.e. 2 hours) following the previously been used to understand relationships between last measured precipitation. We then classified precipitation body composition, energetics and migration in birds and bats events as storms if the total precipitation during the event was (e.g. McGuire et al., 2018; Kelsey et al., 2019; Guglielmo greater than one standard deviation above the mean amount et al., 2022). Furthermore, the use of QMR to quickly and of precipitation that fell during all rainfall events in the study accurately quantify the body composition of live animals has (similar to the > 10 and > 20 mm thresholds for heavy and been validated and is repeatable with < 3% coefficients of strong rainstorms in Skagen and Adams, 2012, Öberg et al., variation for each measure (Guglielmo et al., 2011). 2015). Based on the capture time of the individual, we then determined whether an individual experienced a storm in the Hematocrit 48 hours prior to capture. We collected a ∼ 70 μl blood sample from 263 of the 325 individuals that were scanned in the QMR machine. Blood Statistical methods was drawn from the brachial vein using a 26-gauge needle, To identify whether weather prior to capture affected body collected in a capillary tube, and kept it on ice for up to composition and hematocrit, we used four generalized addi- ∼ 6 hours. We centrifuged capillary tubes at 14 000 rpm tive models (GAM) with fat mass, total body water, lean for 5 minutes, which separated the red blood cells from mass and hematocrit as response variables. Fat mass, total the plasma, platelets and white blood cells. Hematocrit was body water and lean mass were modelled with a Gaussian measured as the percentage of the blood made up of packed distribution while hematocrit was modelled with a beta dis- red blood cells. tribution because it is a percentage. We used total body mass (to account for the variation in body composition by size), sex Weather metrics (male or female), whether a storm occurred in the 48 hours Air temperature ( C), relative humidity (%) and precipitation prior to capture (0 = no storm, 1 = storm), the average wet (mm) were measured using a Campbell Scientific (CR-10) bulb temperature in the week leading up to capture, and the data logger located at the Konza Prairie Biological Station ordinal date (to account for seasonal changes in weather and (Nippert, 2022). Air temperature and relative humidity were body composition) as predictor variables in all four models. recorded on the hour and precipitation was recorded every The continuous variables (total body mass, average wet bulb 15 minutes. Using equation (1), we calculated the wet bulb temperature and ordinal date) were included as smooth terms temperature ( C) for each hour (Stull, 2011). to account for non-linear relationships with each response variable. For example, the average wet bulb temperature was included as a smooth term because hot and cold extremes 1/2 T = T atan 0.151977(RH% + 8.313659) could be detrimental to energy stores while ordinal date was included as a smooth term because body composition and + atan (T + RH%) − atan (RH% − 1.676331) hematocrit may vary non-linearly across the breeding season. 3/2 + 0.00391838(RH%) atan (0.023101RH%) To explore the sensitivity of our results to alternative − 4.686035. (1) modelling approaches, we repeated our modelling efforts while varying how we controlled for body size. We compared Wet bulb temperature (T ) is a function of temperature models that included total body mass, tarsus and both total (T) and relative humidity (RH%) and is used as a measure body mass and tarsus to models with no control for body size of heat stress (e.g. Kang et al., 2020) because it takes into using AICc (methods outlined in the Supplemental materials). account how heat dissipation and evaporative cooling can We report the results of the models that included total body differ based on both temperature and humidity. Furthermore, mass below because the top models consistently contained .......................................................................................................................................................... 4 Conservation Physiology • Volume 11 2023 Research article .......................................................................................................................................................... mass as a predictor. Models that included tarsus performed similarly to models that contained no measure of body size or mass (Supplementary Tables S1 and S2). We used the package ‘mgcv’ (Wood, 2011, 2017) to per- form the analysis in R (version 4.1.1, R Core Team 2021). Results We captured grasshopper sparrows from early May to the end of July in 2014–16 (earliest capture date, May 2; latest capture date, July 29). A total of 325 individuals were captured of which, 48 were female and 277 were males. Individuals had an average total body mass (± standard deviation [SD]) of 17.15 ± 0.86 g (range = 14.94–20.16 g) and total body mass was constant throughout the breeding season (Pearson’s correlation: r = −0.08, P = 0.17). Grasshopper sparrows had an average fat mass of 0.64 ± 0.23 g (range = 0.04–1.58 g), an average total body water of 11.98 ± 1.58 g (range = 0.28– 17.72 g) and an average lean mass of 14.08 ± 0.84 g (range = 8.09–16.29 g). Hematocrit ranged between 40% and 59% with a mean of 50.05 ± 3.02%. During the breeding season, the wet bulb tempera- ◦ ◦ ture ranged from −4.88 C to 28.92 C (mean ± SD in ◦ ◦ 2014 = 15.20 ± 6.89 C, 2015 = 16.47 ± 6.23 C and 2016 = 16.35 ± 6.43 C) and increased throughout the breeding season (Pearson’s correlation: r = 0.67, P < 0.001). Total rainfall during the breeding season varied substantially between the 3 years (2014 = 343.80 mm, 2015 = 515.80 mm, 2016 = 464.20 mm) and was unpredictable within the breeding season (Pearson’s correlation: r = −0.07, P = 0.24). Rain falling in individual precipitation events ranged from ff 0.30 to 96.60 mm (mean = 6.68 ± 11.53 mm) with events lasting between 15 minutes (the shortest detectable time) and 24.5 hours. Precipitation events were considered storms if rainfall exceeded 18.21 mm. Across the 3 years, there were 62 individuals that experienced a storm in the 48 hours prior to capture. In total, there were 18 storms that occurred during the three breeding seasons (May–July; 2014 = 5, 2015 = 8, 2016 = 5 storms), 10 of which occurred within 48 hours prior to a capture event. Predictors of body composition and hematocrit Grasshopper sparrows that were exposed to storms in the 48 hours prior to capture on average had 0.08 g less fat (± 0.03 SE, P = 0.01), 0.44 g more water (± 0.17 SE, P = 0.01) and 0.15 g more lean mass (± 0.07 SE, P = 0.03) than those that did not recently experience a storm (Table 1, Fig. 1A–C). Similarly, a storm prior to capture was also associated with higher hematocrit (0.03 ± 0.02 SE, P = 0.05, Table 2, Fig. 1D). Individuals exposed to elevated wet bulb temperatures in the week prior to capture had larger fat stores (P = 0.02) than individuals exposed to more moderate temperatures (Fig. 2). .......................................................................................................................................................... Table 1: Output from three generalized additive models (family = Gaussian, link = identity) used to assess the relationship between the body composition of 325 grasshopper sparrows (A. savannarum) and whether an individual experienced a storm prior to capture Fat mass Total body water Lean mass Parametric parameters Estimate ± SE tvalue P Estimate ± SE tvalue pvalue Estimate ± SE t value P Intercept 0.77 ± 0.03 24.66 < 0.001 11.80 ± 0.18 64.31 < 0.001 14.01 ± 0.07 189.79 < 0.001 Sex −0.12 ± 0.03 −3.73 < 0.001 0.11 ± 0.20 0.58 0.56 0.06 ± 0.08 0.72 0.47 Storm pre-capture −0.08 ± 0.03 −2.80 0.01 0.44 ± 0.17 2.58 0.01 0.15 ± 0.07 2.21 0.03 Smooth parameters edf F Pvalue edf F pvalue edf F pvalue Mass 3.06 13.30 < 0.001 1.00 79.68 < 0.001 3.67 139.35 < 0.001 Temperature 1.00 5.55 0.02 1.00 1.66 0.20 1.00 0.07 0.79 Ordinal date 1.00 0.02 0.89 7.92 17.28 < 0.001 2.22 2.74 0.05 The three response variables (fat mass (g), total body water (g) and lean mass (g)) were measured using a quantitative magnetic resonance machine. Parametric predictors in each model included the sex of the individual and whether the individual experienced a storm prior to capture (binary: no or yes). Smooth term predictors included the total body mass (g) of the individual, the average wet bulb temperature in the week leading up to capture, and the ordinal date of capture. SE = standard error and edf = eective degrees of freedom. Research article Conservation Physiology • Volume 11 2023 .......................................................................................................................................................... Figure 2: The relationship between the average wet bulb temperature ( C, wet bulb temperature is an index of temperature and humidity) in the week prior to capture and the fat mass (g) of grasshopper sparrows (A. savannarum). Each point represents one individual (n = 325). Figure 1: The relationship between whether there was a storm in the 48 hours prior to capture (yes, darker shade; no, lighter shade) and (A) fat mass, (B) total body water, (C) lean mass and (D) hematocrit of male (blue) and female (grey) grasshopper sparrows (A. savannarum, Discussion n = 325 for A, B and C, n = 263 for D). The black points represent the mean and the whisker represents the standard deviation for each sex. Using 3 years of physiological data collected on wild birds, we provide evidence that individuals modulate their body composition and hematocrit following exposure to severe Table 2: Output from a generalized additive model (family = beta, weather. Individuals that survived and were captured after link = logit) used to assess the relationship between hematocrit of 263 storms carried less fat, retained more water and had higher grasshopper sparrows (A. savannarum) and whether an individual hematocrit than individuals who experienced less extreme experienced a storm prior to capture weather prior to capture. In avian studies, fat is primarily Parametric parameters Estimate ± SE z value P viewed as the energy source used to fuel long, migratory flights (Deppe et al., 2015; Araújo et al., 2019). Our work Intercept −0.03 ± 0.02 −1.54 0.12 suggests that fat deposits may also be used to cope with Sex 0.03 ± 0.02 1.40 0.16 short-term, more acute stressors such as extreme precipita- tion events. This implies that surviving a storm is energet- Storm pre-capture 0.03 ± 0.02 1.93 0.05 ically costly and weather possibly limits foraging options Smooth parameters edf Chi Pvalue to the extent that individuals resort to catabolism of their Mass 1.00 0.77 0.38 fat stores to meet thermoregulatory and other metabolic demands. Temperature 1.82 1.69 0.56 Ordinal date 3.11 10.72 0.02 The high energy expenditure associated with surviving a storm may also explain why hematocrit was elevated in The response variable was hematocrit (bounded by 0 and 1). Parametric predictors in each model included the sex of the individual and whether the individual experi- storm-exposed individuals. High hematocrit has previously enced a storm prior to capture (binary: no or yes). Smooth term predictors included been associated with increased energy demands during migra- the total body mass (g) of the individual, the average wet bulb temperature in the tion (Krause et al., 2016a), winter acclimatization (reviewed week leading up to capture, and the ordinal date of capture. SE = standard error by Fair et al., 2007) and reproduction (Lownie et al., 2022). and edf = eeff ctive degrees of freedom. We suggest hematocrit may even be modulated to assist with surviving severe weather via two potential mechanisms. First, As the breeding seasons progressed, individuals held more to survive storms, birds must thermoregulate during wet and water (P < 0.001), had a higher lean mass (P = 0.05; Table 1) damp conditions, potentially even with wet feathers. To meet and had lower hematocrit (P = 0.02; Table 2). Females had the energetic and oxygen demands of thermogenesis, birds can 0.12 g more fat than males (± 0.03 SE, P < 0.001), but the quickly upregulate erythropoiesis and modulate their hema- sexes did not differ in body water, lean mass or hematocrit tocrit by producing and releasing reticulocytes (young red (Tables 1 and 2). blood cells) into the bloodstream (Campbell and Ellis, 2013). .......................................................................................................................................................... 6 Conservation Physiology • Volume 11 2023 Research article .......................................................................................................................................................... Reticulocytes are larger than erythrocytes (Campbell and because we did not see a correlation between ordinal date Ellis, 2013) and can therefore lead to elevated hematocrit. and fat mass nor total body mass, this explanation is less Alternatively, elevated hematocrit could also indicate that likely. Additionally, our results contradict previous work on the birds were dehydrated post-storm. Dehydration leads to the energetic stress hypothesis that mass, and therefore, fat a larger proportion of the blood being composed of red and lean mass should decrease throughout breeding (Rick- blood cells and more viscous blood due to reduced plasma lefs, 1974; Merila and Wiggins, 1997; Boyle et al., 2012). volume (Zhou et al., 1999). However, total body water was However, because we do not know where each individual higher in birds exposed to a storm so dehydration is less was in the timing of their breeding activities, and because likely as an explanation for elevated hematocrit following a the grasshopper sparrows may re-nest several times within a storm. Overall, while high hematocrit can mean an increased single breeding season, we cannot draw connections between aerobic capacity, if hematocrit is too high, it could make birds the energetics of reproduction and our measures of body and other endotherms susceptible to extreme heat due to a composition. decreased ability to manage internal temperatures via heat Contrary to our prediction, birds exposed to storms had loss (Zhou et al., 1999). higher lean mass than birds that experienced average weather How endotherms, including birds, respond to elevated conditions. Lean mass, composed of muscles and organs, rep- temperatures is relatively well understood. Here, we build on resents another source of energy that birds may rely upon to previous results of the relationship between temperature and survive. Thus, we predicted that individuals may break down avian physiology by considering how temperature and humid- proteins for energy and have lower lean mass following severe ity work together (i.e. wet bulb temperature). Grasshopper weather. We suspect that because our estimate of lean mass sparrows that experienced warmer wet bulb temperatures also includes a large proportion of water content (Boyle et al., in the week prior to capture had more fat than those that 2012), our observation of elevated total body water following experienced cooler weather. Warmer temperatures may allow a storm is most likely driving higher lean mass. Alternatively, for more foraging opportunities with increased prey activity survivor bias could be skewing results whereby individuals and availability (e.g. Asmus et al., 2018), enabling individuals with lower lean mass either did not survive the severe weather, to grow and maintain fat stores. Throughout the majority or they dispersed to avoid exposure. Another non-mutually of our study, the temperatures that birds experienced were exclusive explanation could be that individuals either prepare well within their thermoneutral zone (estimated upper limit, for, or following a storm, try to recoup losses in fat stores ◦ ◦ 38.7 C and heat tolerance limit, 45.2 C for temperate birds; by foraging more and thus have fuller gastrointestinal tracts. Pollock et al., 2021). The maximum average wet bulb tem- However, passage of food through the gastrointestinal tracts perature during this study was 28 C and the maximum air of birds is rapid (1–2 hours in several species of sparrow; temperature recorded was 39.48 C. The days where air tem- Stevenson, 1933), that is why the timing of the estimation of peratures potentially exceeded the thermoneutral zone were body composition post-storm is important. A study at a finer few: 6 days in 2014, 0 days in 2015, and 3 days in 2016. scale than our 48-hour window is necessary to elucidate the Thus, it is unlikely that we would observe individuals who relationship between storms and lean mass and an immediate were depleting their energy stores as a result of thermoreg- measure of body composition post-storm would provide a ulatory stress. Furthermore, wet bulb temperature was not better indication of how individual’s energy stores are used associated with differences in total body water or hematrocrit, to survive extreme weather. further suggesting that elevated temperatures did not lead to Our results indicate that individuals may modulate their dehydration. body composition and hematocrit following both an acute, In our analyses, we controlled for ordinal date to account severe precipitation event and a more prolonged span of ele- for intra-annual changes in temperature and precipitation. vated temperature and humidity. This suggests that individual Throughout the breeding season, total body water and lean body composition, in particular fat stores, are sensitive to a mass increased, hematocrit declined and total body mass and range of environmental conditions. Historically, most work fat mass did not vary over time. The observed shift in total investigating avian fat stores, lean mass and hematocrit are body water and lean mass but not fat mass may be a result conducted in the winter (Houston and McNamara, 1993; of increasing temperatures, declining water availability, or Bednekoff and Houston, 1994) or during migration (King shifts reproductive behaviour and therefore energy expen- and Farner, 1965; Cooper et al., 2015). Focusing on more diture throughout the season. Individuals may respond to rapid changes in body composition (e.g. hours or days) would drier conditions by storing more water endogenously (e.g. complement past 0research examining longer term changes Bartholomew and Cade, 1963), leading to higher body water in body composition (e.g. across entire seasons) and could be and potentially wet lean masses. Alternatively, lean mass may achieved by repeatedly sampling individuals pre- and post- increase throughout the summer because energy stores could storms. Expanding these studies to other periods of the annual have been depleted following spring migration but rebuilt in cycle and different temporal scales could help to elucidate time for fall migration. However, because birds are capable of how individuals augment their body composition in response rebuilding fat and lean mass quickly (days to weeks instead to a wider range of environmental conditions and acute of over an entire season) particularly prior to migration, and stressors to better predict individual performance. .......................................................................................................................................................... 7 Research article Conservation Physiology • Volume 11 2023 .......................................................................................................................................................... The rise in global temperatures and shifts in the frequency Supplementary material and intensity of precipitation (IPCC 2022) has consequences Supplementary material is available at Conservation Physiol- and may push wildlife towards their physiological limits to the ogy online. detriment of fitness. Such consequences are already present where breeding birds in arid regions are no longer able to maintain their own condition let alone provision offspring (e.g. Silva et al., 2015; van de Ven et al., 2019). Here, References we show that high temperatures, reduced total precipitation and increased severity of storms may impact small-bodied Albright TP, Mutiibwa D, Gerson Alexander R, Smith EK, Talbot WA, endotherms body composition and their aerobic capacity. 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Journal
Conservation Physiology – Oxford University Press
Published: Mar 20, 2023
Keywords: QMR; precipitation; lean mass; fat stores; energetics; body composition