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Arousal Patterns, Metabolic Rate, and an Energy Budget of Eastern Red Bats (Lasiurus borealis) in Winter

Miranda B. Dunbar, Thomas E. Tomasi
DOI: http://dx.doi.org/10.1644/05-MAMM-A-254R3.1 1096-1102 First published online: 29 December 2006

Abstract

Eastern red bats (Lasiurus borealis) will move into leaf litter during cold bouts of winter, and because temperatures fluctuate at these roosts, our 1st goal was to quantify winter arousals in response to ambient temperature (Ta). Additionally, we measured changes in metabolism and body temperature (Tb) during hibernation and arousals at various Ta. Using these data, we estimated winter energy budgets. Bats were captured during autumn of 2003 and 2004 in southwestern Missouri and kept in environmental chambers simulating natural conditions. We assessed torpor bout duration using temperature-sensitive data-loggers within environmental chambers at 15°C, 10°C, 5°C, and 2°C. Metabolic rate during torpor was assessed within metabolic chambers at 15°C, 10°C, 5°C, 1°C, and −5°C. Examination of our data suggests that torpor bout duration was not affected by sex and it was inversely related to Ta down to 2°C. Metabolic rate during torpor was not affected by sex but it did vary with Ta. Tb of hibernating bats approximated Ta and the difference between these was greatest at 1°C. Our studies of thermal physiology provide insight of overwintering behaviors of L. borealis, which are apparently less constrained by thermal parameters than in other temperate bat species.

Key words
  • arousals
  • bat
  • energetics
  • hibernacula
  • hibernation
  • metabolic rate
  • thermoregulation
  • torpor

During daily or seasonal periods of inactivity, many mammals employ heterothermic mechanisms that allow them to conserve energy. Torpor, one of these mechanisms, is typically categorized as either shallow (daily) torpor or prolonged (seasonal) torpor (synonymous with hibernation—Geiser and Ruf 1995). Both physiological states involve decreases in physiological parameters (e.g., oxygen consumption rate, heart rate, and body temperature [Tb]); however, the decreases during hibernation are generally of a greater magnitude (Lyman 1948). Geiser and Ruf (1995) suggest that maximum duration of torpor bouts and minimum metabolic rate are the parameters best suited for classifying torpor patterns. Most commonly, torpor is used to minimize thermoregulatory costs during periods of extreme conditions such as low ambient temperature (Ta) and decreased food availability and its benefits may differ between sexes. For example, hibernation may assist in further delaying fertilization in females, but this may not be requisite (Racey and Entwistle 2000), and daily torpor during summer may be minimized via microhabitat selection in pregnant or lactating females to expedite development of offspring (Cryan and Wolf 2003; Grinevitch et al. 1995; Willis and Brigham 2005).

Hibernation is not a static physiological state (French 1985) and hibernating mammals periodically arouse, presumably to allow physical or biochemical events to occur during the subsequent euthermic period (Park et al. 2000), although the trigger for arousal is unknown. Regardless of the cause, arousal is energetically expensive in terms of caloric need. Frequent spontaneous arousals without energy intake will result in rapid loss of mass, leaving insufficient reserves for thermoregulation. Therefore, arousal duration and frequency are important elements when considering the total winter energy budget, especially in small hibernators such as bats.

For non-cave-dwelling bats, choosing effective hibernacula presents a challenge because fluctuating environmental conditions may threaten energy reserves. Hibernating during periods of low Ta requires roost temperatures below an individual's thermoneutral zone, thus allowing the body to cool and metabolism to decrease (Schmidt-Nielsen 1990). However, hibernacula temperatures below freezing require an increase in metabolism to maintain Tb above freezing. Other studies suggest that some non-cave-dwelling insectivorous bats select hibernacula where temperature is more stable than but still correlated with Ta (Ransome 1968, 1971, 1995).

The eastern red bat (Lasiurus borealis; henceforth red bat) is a widely distributed, foliage-roosting species found throughout the eastern United States, southern parts of Canada, and northern Mexico (Shump and Shump 1982). Davis and Lidicker (1956) and Whitaker et al. (1997) suggested that L. borealis commonly winters in regions where freezing temperatures are frequently encountered. Cryan (2003) suggested that L. borealis is a migratory species, because it appears to winter in southeastern North America; however, males remain common in northern areas during winter. Red bats winter in southwestern Missouri where subfreezing temperatures occur, although it is not knowrr whether these individuals are migrants or year-round residents. Boyles et al. (2003) demonstrated that winter capture success of red bats in this area is correlated to changes in Ta.

Unlike most hibernating bats, L. borealis does not use typical hibernacula (e.g., caves); instead, they remain in tree canopies during relatively warm winter days and move into leaf litter on the forest floor during cold bouts of winter months (Boyles et al. 2003; Moorman et al. 1999; Saugey et al. 1998). This is supported by observations that red bats on several occasions emerged from leaf litter in January and February (Moorman et al. 1999) and early May (Rodrigue et al. 2001) in response to approaching prescribed burns. These sites for hibernation may be beneficial for energy conservation because they provide a relatively stable microhabitat (Hutchinson and Lacki 2001; Mager and Nelson 2001) while protecting bats from other winter climatic effects (e.g., low humidity, snow, and wind). In addition, leaf-litter sites may provide opportunities for passive rewarming, thus allowing greater energetic savings during arousals from torpor (Geiser et al. 2004). Other suitable characteristics of leaf litter include color (camouflage) and resistance to decay; both likely contribute to the success of a wintering site for L. borealis (Moorman et al. 1999).

Although metabolism and Tb of red bats have been measured during summer and early autumn (Davis and Reite 1967; Genoud 1993; Reite and Davis 1966), their energetics during winter and hibernation are poorly understood. Numerous authors have suggested the need for additional studies of overwintering strategies in hibernating L. borealis (Boyles et al. 2003; Cryan 2003; Davis and Reite 1967; Genoud 1993; Ransome 1971; Reite and Davis 1966). However, few attempts have been made because capturing bats in winter is logistically difficult, as is maintaining bats in captivity for long periods.

Our 1st goal was to assess the relationship between length of torpor bouts and Ta. Second, we measured changes in metabolism and Tb during hibernation and arousals at various Ta common during winter in southwestern Missouri. We evaluated whether torpor use differed between sexes and, by using selected temperatures for a specific location, estimated winter energy budgets for L. borealis. We predicted that arousals from hibernation would be spontaneous (without stimuli), and torpor bout duration would be negatively correlated with Ta. We also predicted that metabolic rate during torpor (TMR) would vary with Ta. Furthermore, we predicted that during hibernation the discrepancy between Tb and Ta would increase as Ta approached freezing.

Materials and Methods

We captured bats in mist nets (Avinet, Dryden, New York) set over shallow creeks and forest corridors at Busiek State Forest (UTM 4048000N, 475000E; Christian County, Missouri) and Drury Mincy Conservation Area (UTM 4047000N, 493000E; Taney County, Missouri). Most bats (n = 18) were collected during September and early October when daily high temperatures averaged 18°C, but we continued mistnetting throughout winter. Six bats died in captivity so we replaced these with additional bats collected later in the winter season. Surviving bats were released subsequent to the hibernation season at the site of capture in March, when daily high temperatures averaged 11°C.

We kept L. borealis in separate enclosures consisting of a soft, netted nylon material supported by a polyvinyl chloride frame measuring 33 × 33 × 33 cm. Leaves from a variety of species of oak (Quercus) and hickory (Carya) were collected, dried, sterilized (via microwave oven), and placed in each enclosure to a depth of approximately 10 cm. All enclosures were kept in an environmental chamber (model DT72LGD; Powers Scientific Inc., Hatboro, Pennsylvania) where temperature and photoperiod mimicked ambient conditions. Water pans within the environmental chambers served to maintain humidity.

During the acclimation period and arousals from hibernation, bats were given mealworms (larval Tenebrio) as food and water was available ad libitum. Feeding times changed according to photoperiod to mimic natural feeding bouts. Bats were induced to hibernate by gradually reducing Ta (20-15°C) and shortening photoperiods.

Once individuals commenced hibernation, we monitored torpor bout durations while sequentially exposing each bat to 4 experimental temperatures (15°C, 10°C, 5°C, and 2°C, each ± 1°C) until most individuals had experienced 4 torpor bouts (5 natural arousals). The time required for bats to experience 5 natural arousals increased as temperature decreased (12-29 days). We measured arousals using temperature-sensitive data-loggers (iButton; Maxim Semiconductors, Dallas, Texas). When a bat was found torpid and under the leaf litter, it was placed on a foam board (approximately 6.4 × 6.4 cm) with an iButton embedded. If a bat moved, this was counted as an arousal and the individual was placed back onto the iButton. To minimize disturbance and handling time, we constructed a simple grid pattern on the floor of each enclosure so that we could track any movement and locate torpid bats that may have changed locations under the leaf litter. At warmer Ta, some bats began to arouse after handling to place them back onto the iButton, but they soon re-entered torpor. Individuals were checked daily at the 15°C treatment, every 3 days at 10°C, every 5 days at 5°C, and weekly at 2°C. The movements, and therefore arousals, of bats that remained hanging rather than entering leaf litter (mostly at higher Ta) also were recorded. An arousal was characterized by a rapid increase in temperature recorded with the iButton. It was common (at lower Ta) to record arousals without apparent movement, suggesting the bat remained in contact with the iButton during euthermic periods and re-entered torpor without changing position. Cooling curves for bats entering torpor while remaining on an iButton were distinct from when a bat had moved off of the iButton and the device had cooled to Ta (Fig. 1). Mean torpor bout duration (in days) was calculated for each individual at each Ta treatment.

Fig. 1

Cooling rates for a warm temperature-sensitive datalogger (iButton) placed in the environmental chamber and for a euthermic Lasiurus borealis entering torpor while remaining on an iButton at 5°C. These differences allowed for identification of arousals where no physical movement was observed, b) A subset of data depicting arousals from L. borealis at 5°C over a 7-day period.

To characterize the physiological effects of temperature, we measured TMR for individual bats at various Ta (15°C, 10°C, 5°C, 1°C, and −5°C, each ± 1°C). Metabolism was measured as the rate of oxygen consumption within an open-airflow metabolic chamber (which consisted of a 50-ml syringe barrel and a large 1-hole cork) using a 2-channel oxygen analyzer (S-3A/II; Applied Electrochemistry, Pittsburgh, Pennsylvania). Excurrent air was drawn into the oxygen analyzer at a flow rate of 0.0156 liters/min (0.13043 liters/min for measurements at −5°C) after passing through soda lime and silica gel to remove carbon dioxide and water, respectively. The metabolic chamber temperature was measured with a Teflon insulated probe, and was controlled by placing the metabolic chambers in either a 3-liter insulated Plexiglas box in a water jacket (1–15°C) or a freezer (−5°C). Bats were exposed for approximately 24 h at each experimental temperature except −5°C, to which they were exposed for 3 h (after TMR had stabilized and to minimize stress during low-temperature exposure). All trials began during the inactive part of their daily cycle.

Oxygen consumption was recorded at 5-min intervals. Using these data, we calculated the mean amount of oxygen consumed per hour and identified the minimum value (taken from these 1-h means) for each metabolic experiment for each individual. Metabolic rates were calculated following Hill (1972) and corrected to ambient pressure, but not standard temperature (because air was drawn through the oxygen analyzer before the flow rate was determined). Data were analyzed for whole animal (O2 ml/h), and were also adjusted per gram (O2 ml h−1 g−1; for comparison to literature values) and as mass-independent values (O2 ml h−1 g−0.67; to remove the effect of body mass). We used 0.179 O2 ml/h = 1 mW for conversion to SI units.

During some metabolic measurements, we simultaneously measured rectal temperature with a quick-response Teflon insulated thermocouple probe measuring 0.023 cm in diameter. After insertion, thermocouple wires were taped to the dorsal surface of individuals to prevent bats from removing thermocouple wires.

Using the data for arousal frequency and duration (h), torpor duration (h), and metabolism (O2 ml/h) we calculated total winter energy budgets for 15°C, 10°C, 5°C, and 1°C. For these calculations, we defined the hibernation season as 135 days (November 1 through March 15). We calculated total cost of arousals by multiplying duration of 1 arousal (h) by metabolic rate during the arousal (O2 ml/h). After multiplying this result by the estimated total number of arousals per season, we were able to estimate the cost of euthermia. Calculations were repeated for total metabolic costs during torpor. We converted total torpid and arousal metabolic values into kilocalories (0.004825 kcal/O2 ml) and kilojoules (4.184 kJ/kcal) and then ultimately into fat mass (9.4 kcal/g) to estimate the amount of body fat lost.

We used a 2-way analysis of variance (ANOVA; general linear model procedure) to examine the effects of sex and Ta on torpor bout duration and TMR. There was no sex effect or sex × Ta interaction for either parameter so we pooled the data and used 1-way ANOVA and Tukey's tests to assess the effects of Ta. These analyses were repeated including only males because of the small sample size of females and because behavioral observations of activity varied between sexes. All statistics were calculated using Minitab Version 14 (Minilab Inc., State College, Pennsylvania) and we employed an alpha value of 0.05.

Our protocols followed guidelines for animal use in research set forth by the American Society of Mammalogists (Animal Care and Use Committee 1998) and were approved by the Missouri State University Institutional Animal Care and Use Committee.

Results

Red bats (n = 21 males; n = 3 females) were captured in southwestern Missouri in most winter months; however, no females were captured after October.

For our periodic arousal experiment, there was no effect of sex on torpor bout duration (F = 0.61, d.f. = 1, P = 0.441) and no sex × Ta interaction (F = 0.75, d.f. = 3, P = 0.531). for pooled data, torpor bout duration was negatively correlated with Ta (F = 48.02, d.f. = 3, P < 0.0005; Fig. 2) and torpor bout lengths were different among temperature treatments (P < 0.05). In males, torpor bout duration varied similarly with Ta (F = 38.36, d.f. = 3, P < 0.0005) and was longer at both 1°C and 5°C than at all other higher Ta (P < 0.05). There was no difference in torpor bout duration for males between Tas of 10°C and 15°C (P < 0.05).

Fig. 2

Duration of torpor bouts for Lasiurus borealis in response to ambient temperature (Ta). Data are pooled for sex and presented as mean ± 1 SE with 2nd-order regression (torpor bout duration = 9.415 − 0.972(Ta) + 0.03 l(Ta)2). Numbers above standard error bars are number of individual bats. Torpor bouts are shorter at higher Ta (P < 0.0005) and different among all Ta treatments (P < 0.05).

In our respirometry trials, there was no effect of sex on TMR for whole-animal (O2 ml/h: F = 0.00, d.f. = 1, P = 0.971), mass-specific (O2 ml h− 1 gh−1: F = 1.80, d.f. = 1, P = 0.191), or mass-independent (02 ml h−1 g−0.67: F = 0.88, d.f. = 1, P = 0.357) values and no sex × Ta interaction for whole-animal (O2 ml/h: F = 1.31, d.f. = 4, P = 0.293), mass-specific (O2 ml h−1 g−1: F = 2.54, d.f. = 4, P = 0.064), or mass-independent (O2 ml h−1 g−0.67: F = 2.10, d.f. = 4, p = 0.110) values. When pooled across the sexes, Ta affected TMR for whole-animal (O2ml/h: F = 18.31, d.f. = 4, P < 0.0005; Fig. 3), mass-specific (O2 ml h−1 g−1: F = 12.79, d.f. = 4, P < 0.0005), and mass-independent (02 ml h−1 g−0.67: F = 14.40, d.f. = 4, P < 0.0005) values. Regardless of how it is expressed, TMR at −5°C was higher than at all other temperature treatments (P < 0.05) and higher at 15°C than at 5°C and 10°C (P < 0.05). In males, regardless of how it is expressed, TMR at −5°C was higher than at all other temperature treatments (P < 0.05).

Fig. 3

Whole-animal metabolic rates of torpid Lasiurus borealis in response to ambient temperature (Ta). Data are pooled for sex and presented as mean ± 1 SE. Numbers above standard error bars are number of individual bats. Ta affected metabolic rates during torpor (P < 0.0005). Metabolic rate during torpor at -5°C was higher than at all other temperature treatments (P < 0.05), and at 15°C it was higher than at 5°C and 10°C (P < 0.05).

Rectal insertion of a thermocouple typically triggered arousal and bats often damaged thermocouples by chewing, so we could not obtain Tb data for all individuals. However, the data obtained for 2 trials at 1°C, 1 trial at 5°C, and 3 trials at 10°C indicated that torpid Tb of all individuals remained approximately 0.4–1 °C above most Ta and the discrepancy between these was greatest at 1°C (approximately 2°C above Ta).

Arousals were most costly in total energy expenditure at 15°C, where arousals occur most often, and least costly at 1°C, where arousals are much less frequent (Table 1). Total energy expenditure during torpor was greatest at 15°C and least at 5°C (Table 1). Lastly, total predicted fat mass loss (g) at 15°C was higher than all other temperatures (Table 1).

View this table:
Table 1

Estimated winter energy budget for Lasiurus borealis at selected temperatures. The hibernation season was defined as 135 days. Numbers in square brackets [n ] are number of natural arousals recorded during metabolic experiments. Total metabolic costs were converted into equivalent fat mass (g; see text for calculations).

Ambient temperature
1°C5°C10°C15°C
Arousal durationa (h), [n ]1.08 [1]6.75 [1]1.83 [2]1.67 [2]
Euthermic metabolic ratea as O2 ml/h27.2824.0731.8837.07
No. arousals per season16.7627.6239.4283.87
Total cost of arousals per season (kJ)10.0090.5846.53104.60
Time torpid per season (h)3,221.843,053.573,167.743,100.22
Torpid metabolic rate as O2 ml/h0.930.380.412.37
Total cost of torpor per season (kJ)60.2523.1826.23148.36
Total cost per season (kJ)70.25113.7672.76253.01
Total cost in equivalent fat mass per season (g)1.792.891.856.43
  • a These data were approximated because of small sample sizes, O2 levels not being recorded below 15% of room air (because of hardware or software malfunction), and costs of euthermic activity (flying, digestion, etc.) not being considered.

Discussion

The low capture rate of females during winter provided unequal sample sizes between the sexes, which may have masked sex differences in measured parameters. Variation in capture rates between males and females suggests sex-biased migration or different overwintering strategies in southwestern Missouri. Cryan (2003) suggested that it is common for male and female bats to differ in distribution at both limited and larger scales during winter.

We found that torpor duration was inversely correlated with Ta (Fig. 2) and L. borealis may use this relationship to exploit food availability by foraging on warm winter nights. In support of this, fresh food samples were found in the fecal matter of several L. borealis captured in southwestern Missouri during winter of 2004–2005, demonstrating that these bats continue to forage during winter months. It is advantageous in relation to foraging success for bats to have frequent arousals at higher Ta (Park et al. 2000) because insect abundance (and therefore, potential energy gain-Speakman and Racey 1989) increases as Ta increases (Jones et al. 1995). However, we would expect this same pattern in hibernators that do not feed. A critical temperature in regard to foraging may exist above which feeding during arousals should be profitable and below which remaining inactive during arousals should minimize energy losses (Avery 1985).

Hibernaculum selection may be important by allowing appropriate timing of arousals for ambient conditions (Ransome 1971; Speakman and Racey 1989). Leaf litter may provide a good compromise for red bats because it provides some thermal buffering from Ta extremes while also allowing individuals to monitor ambient conditions to identify potential foraging opportunities. The arousal patterns we recorded occurred in constant conditions, but, in a natural setting, fluctuations of Ta may allow bats to passively rewarm from torpor.

Although important when predicting the duration and timing of arousals, foraging is not likely the primary function of arousals (Park et al. 2000). For example, metabolic imbalances (i.e., waste accumulation) need to be corrected less often in cooler temperatures, which may thereby yield similar arousal patterns. Because we captured L. borealis in southwestern Missouri in winter months when insect activity is unlikely (4–5°C), this suggests other reason(s) for flight during an arousal. Other suggested functions of activity during arousals in hibernating bats include (but are not limited to) finding water for rehydration (Fisher and Mannery 1967; Speakman and Racey 1989; Thomas and Cloutier 1992; Thomas and Geiser 1997), reproductive activities (Tidemann 1982), and roost-site selection (Ransome 1968, 1971).

In our study, TMR was lowest at 5°C (representing the greatest energy savings) and bats increased metabolism at 15°C and 1°C (Fig. 3), even though length of torpor bouts continued to increase below this temperature. Below 1°C, there was an even larger increase in TMR. Theoretically, TMR would exponentially increase above an optimal temperature and linearly increase below this. Therefore, a low Ta (i.e., 5°C) appears optimal (energetically) for hibernating red bats. The closer the actual Ta is to this optimal Ta, the lower the metabolic rate, thus allowing greater energy savings (Davis 1970; McNab 1974; Nagel and Nagel 1991).

Body temperature of thermoconforming torpid animals approximates Ta until Ta drops below a “defended” minimum set point (Hock 1951). In our study, bats responded to decreasing Ta below 5°C by increasing metabolism to maintain Tb above this defended level. Further increasing metabolism (i.e., in response to decreasing Ta) may trigger an arousal, thereby using more energy than thermoregulation during dormancy. Likewise, Reite and Davis (1966) demonstrated an increase in the difference between the rectal temperature of hibernating L. borealis and Ta as Ta decreased. During the −5°C treatment in our study, bats either increased metabolism (presumably to keep Tb above Ta; n = 2), exhibited an arousal most likely triggered by the decrease in Ta, or remained passive and froze to death.

We estimated the total winter energy budget and potential body fat losses at selected temperatures (Table 1). For these calculations, Ta was assumed to remain constant for the entire hibernation season. Although this is unrealistic, it provides a range of values that likely encompass the actual cost. We did not calculate an estimate for −5°C because bats typically aroused during this experimental temperature and remained euthermic. This temperature appears to be below the thermal limit for hibernation by this species.

Arousal patterns were most beneficial (in terms of metabolic costs) if low in frequency (as seen at 1°C). Frequent arousals may be profitable if bats are allowed to forage, but this is only possible if Ta is warm enough that insects are available. Duration of arousals also may have a large impact on the total winter energy budget and activity during arousals may dictate their length. Total energy expenditure was highest at 15°C, but this would not likely affect survival because foraging opportunities would exist and fat stores could be replaced. Arousal duration was shortest at 1°C; TMR was most costly at this temperature (of those in Table 1) so short arousal duration may compensate for this cost. Arousal duration was longest at 5°C; this temperature is least costly while torpid so this conserved energy may allow bats to prolong arousals. However, no purpose of a prolonged arousal is suggested, because foraging is likely unprofitable at this temperature. Because of the small sample size of natural arousals demonstrated at this temperature (n = 1), this arousal duration value may not be representative of typical behavior.

Refining winter energy budgets will provide insight to the overwintering behaviors and strategies of red bats, which are apparently less constrained by thermal parameters than are other temperate bat species. Given their hibernacula, red bats will benefit from the relationship between Ta and torpor bout duration, arousing more often during evenings when food is available. We predict that, for red bats hibernating at more northern latitudes where winter feeding opportunities are rare, lower Ta would lengthen torpor bouts and decrease TMR, such that their energy-expenditure patterns would more closely resemble those of cave-dwelling species. At more southern latitudes, where insects are available nightly, the same relationships would generate an energy-expenditure pattern more akin to daily torpor. The plasticity shown by red bats suggests that a latitudinal continuum between classic hibernation and daily torpor may exist in this species. We predict that similar patterns could exist for other species with large geographic ranges in winter, particularly those that roost in relativity exposed locations.

Future work on red bat hibernation could help determine the selection pressure(s) governing variation in overwintering strategies (e.g., hibernation versus migration). Delineating the habitats and climates where hibernating in the leaf litter is advantageous may provide information about habitat-selection strategies. This should contribute to conservation efforts because it will allow for better scheduling of prescribed burns and improved habitat and forestry management. Further assessment of differences in overwintering strategies between the sexes also is needed. We caught very few females in the winter months, which suggests that females rely more heavily on torpor than males during hibernation or that females migrate further south than males during winter. Quantifying winter activity and torpor patterns of different populations hibernating in varied climates also would improve our understanding of the role of sex as an influence on overwintering strategies in temperate bats.

Acknowledgments

We thank L. W. Robbins for early discussions on project design. J. G. Boyles, R. M. Brigham, and 2 anonymous reviewers provided helpful comments on earlier drafts. The Missouri State University Graduate College, Missouri State University Biology Department, and a Missouri State University Faculty Research Grant (to TET) supported this research. The Missouri Department of Conservation allowed access to Busiek State Forest and Drury Mincy Conservation Area for capture and release of bats intended for research. We also thank C. C. Schoppet-Mann, C. M. Dzurick, and A. A. Scesny for assistance with captive care of bats.

Footnotes

  • Associate Editor was Rodrigo Medellín.

Literature Cited

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