Limits to sustained energy intake : I. Lactation in the laboratory mouse MUS MUSCULUS
Aberdeen Centre for Energy Regulation and Obesity (ACERO), Department of Zoology, University of Aberdeen, Aberdeen AB24 2TZ, Scotland, UK
*Author for correspondence (e-mail: j.speakman{at}abdn.ac.uk)
Accepted March 11, 2001
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Summary |
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Key words: energetics, maximal metabolic rate, sustained metabolic rate, pregnancy, lactation, reproduction, mouse
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Introduction |
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A potential area of confusion is that some studies have measured energy expenditure directly to evaluate sustainable metabolic rates (for reviews, see Nagy et al., 1999; Speakman, 2000), but other studies have employed food intake (e.g. Hammond et al., 1994). When animals are at stable body mass, food intake provides an estimate of sustainable metabolic rate because the majority of ingested energy is metabolised, and demonstrated limits on food intake would translate to limits on expenditure. This link between food intake and energy expenditure, however, breaks down when there is substantial export of energy, such as occurs during lactation (see discussion in Speakman and McQueenie, 1996; Speakman, 2000). In this situation, limited food intake still reflects an absolute maximum potential level of expenditure, but actual expenditure will be substantially lower and may be limited at some lower threshold. In the present study, we have also measured food intake as an indicator of sustainable maximum metabolic rate, but use the term sustainable energy intake (SusEI) to emphasize the potential contrast to SusMR.
Limits on SusEI and SusMR are likely to be particularly important during peak lactation, which is the time of greatest energy demand on female mammals (Kenagy et al., 1990; Thompson, 1992). Limitations on SusEI at this time may determine the total investment that mammals can make in their offspring and may, thus, define maximum litter and offspring sizes. Lactating laboratory mice (Mus musculus L.) provide a convenient model animal in which to investigate limitations on SusEI and SusMR, and there have been many recent studies of this system (Hammond and Diamond, 1992; Hammond and Diamond, 1994; Hammond et al., 1994; Hammond et al., 1996; Speakman and McQueenie, 1996). In addition, many earlier studies quantified food intake during lactation in this species (Bateman, 1957; Myrcha et al., 1969; Studier, 1979; König et al., 1988), although not in the context of the theories of sustainable metabolic rates.
Several manipulations have been performed on lactating mice to investigate where limits occur in this system. Swiss Webster mice have been shown to raise a maximum of 14 pups (even though some litters were manipulated up to 26 pups), with the lactating females increasing their food intake throughout lactation and with increasing litter size (Hammond and Diamond, 1992). Hammond and Diamond (Hammond and Diamond, 1994) extended the duration and level of demands placed on the lactating mother by restricting the access of pups to food until they were 21 days old, and found that the mothers did not respond by elevating their food intake above that achieved by mothers raising 14 pups during a normal lactation. However, when lactating mice were also challenged with cold-exposure, they were able to increase their food intake further (Hammond et al., 1994). By surgically manipulating the number of teats on lactating female mice, Hammond et al. (Hammond et al., 1996) found that females with only two teats were unable to raise any pups, and that females with five and 10 teats with the same mammary pressure (pups per teat) raised pups that did not differ in their body masses, even though the mothers with five teats had only half the number of pups to raise.
Overall, these experiments suggest that lactating mice are limited peripherally at the mammary gland in their milk output and regulate their food intake to match this limit. This interpretation is supported by several previous studies of milk production in small mammals. These have shown that, although females with larger litters can produce more milk than those with smaller litters, this is generally insufficient to support the growth rates observed in small litters and, hence, that pups from larger litters are often lighter (Russell, 1980; Meyer et al., 1985; Knight et al., 1986; Fiorotto et al., 1991; Rogowitz and McClure, 1995; Rogowitz, 1996; Rogowitz, 1998).
There is some evidence that different strains of laboratory mice may respond differently to the sustainable limit. The Swiss Webster mice studied by Hammond and Diamond (Hammond and Diamond, 1992; Hammond and Diamond, 1994) and Hammond et al. (Hammond et al., 1994; Hammond et al., 1996) had a maximum food intake of 19g in late lactation and raised a maximum of 14 pups in their first lactation (Hammond and Diamond, 1992). Yet MF1 mice eat up to 26g and raise up to 16 pups in their first lactation (Speakman and McQueenie, 1996). Moreover, the relationship between food intake and litter size for this latter strain does not appear to reach an asymptote (Speakman and McQueenie, 1996) in the range of natural litter sizes, indicating that limits may be set at much higher levels in this strain. In the light of these strain differences, we aimed to investigate the limitations on food intake during lactation in the MF1 mouse and to evaluate how these limitations relate to milk output and the demands of the offspring. An asymptote in maternal food intake with increasing litter size would be consistent with the central limitation hypothesis, whereas an asymptote in milk energy output would be consistent with the peripheral limitation hypothesis.
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Materials and methods |
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One hundred and eight females were paired with males for 6 days, after which the males were removed. Pregnancy was detected by an increase in mass over the following 7 days. Following parturition (day 0), 71 of the females were allowed to raise a natural litter to peak lactation (day 18 of lactation). These females were termed the control females. The remaining 37 females (manipulated) had their litter size manipulated by cross-fostering on day 0 so that they raised more or fewer offspring than they gave birth to. This extended the range of natural litter sizes, which varied from five to 15 pups (control) to between three and 18 pups (manipulated). Females readily accepted the fostered pups.
Female body mass and food intake were measured (using a Sartorius top-pan balance) prior to breeding and then daily throughout pregnancy and lactation. No measurements were made on the days when a male was present. Food intake was calculated as the mass of food missing from the hopper each day. The bedding was checked for bits of uneaten food, which were weighed and returned to the hopper. We fine sorted, by hand, the bedding of 17 of the lactating mice and found that only 1.7±0.41% (mean ± S.E.M.) of the food missing from the hopper was left in the bedding. Following parturition, the number of pups and the total mass of the litter were also recorded each day. All masses were accurate to 0.01g.
To determine the assimilation efficiency, faeces produced over a 5-day period were collected from nine females prior to breeding and from 16 lactating females between days 10 and 15 of lactation. The faeces were weighed, dried at 60°C (Gallenkamp air-fan oven) for 14 days and reweighed. Total food intake over the same time period was also measured. Gross energy content was determined for faeces from non-breeding females (N=5) and lactating females (N=6) and for the food by adiabatic bomb calorimetry (Gallenkamp Autobomb, Rowett Research Institute Analytical Services, Aberdeen, UK). Assimilation efficiency was expressed as the total gross energy intake minus the energy in faeces divided by the total gross energy intake.
Energy expenditure of the litters
On day 13 of lactation, the resting metabolic rate of 10 entire litters was measured using an open-flow respirometry system connected to a paramagnetic oxygen analyser (Servomex model 1100A), as described previously (Hayes et al., 1992; Speakman and McQueenie, 1996). Dry air was pumped (Charles Austin Pumps Ltd) through a sealed Perspex chamber housed inside a constant-temperature incubator (INL-401N-010, Gallenkamp) set at 21°C (the temperature at which the mice were housed). A flow rate of 10001500mlmin-1 was metered continuously using an Alexander Wright flowmeter (DM3A) upstream of the chamber. A sample of the excurrent air leaving the chamber (approximately 150mlmin-1) was dried (silica gel) and directed through the oxygen analyser. Carbon dioxide (CO2) in the outflow was not absorbed prior to measurement of oxygen content, as this provides the most accurate method for measuring energy expenditure (Koteja, 1996; Speakman, 2000) in the absence of a known respiratory quotient (RQ). We calculated the rate of oxygen uptake, .O2, from the product of the downstream oxygen content difference from ambient and the upstream flow rate. As the flow rate was measured upstream of the chamber, oxygen consumption was converted to energy expenditure assuming that RQ=1, using the equation of Weir (Weir, 1949; for calculation details, see Speakman, 2000).
Measurements of the difference in oxygen concentration between ambient and excurrent air were digitised approximately 80 times each second, and the mean was calculated every 30s over a 1h period and stored on a microcomputer (Viglen PC) interfaced with the oxygen analyser. Pups were observed to settle very quickly (within 15min of entering the chamber), and a stable trace was always obtained within the hour. The lowest 5min of oxygen consumption (corrected to STP) was taken as an estimate of the resting metabolic rate (RMR) (mlmin-1). This was converted to an estimated equivalent daily energy expenditure (DEE) (kJday-1), which excludes the costs of any activity.
The total energy requirement (TER) of the litters was assumed to equal the sum of the daily energy expended (DEE) on respiration and the energy diverted to growth, measured from the change in mass of the litters between day 13 and day 14. This was converted to energy (kJday-1) using the calorific value of pups (2.14kcalg-1=8.95kJg-1wetmass; from Brisbin, 1970). Since the TER was based on our estimates of DEE, it also excluded any costs of activity in the litter.
Milk production
Milk production of lactating females was estimated from the difference between the total water turnover and the summed water loss in faeces, urine and by evaporation. This difference was taken to be the volume of water in the milk. Water turnover was measured in 21 lactating females (day 1415 of lactation) by the isotope dilution method using tritiated water (HTO). A blood sample (100µl) was obtained from the females (by taking a 1mm scissor snip from the end of the tail) and flame-sealed in glass capillaries (Vitrex, Camlab Ltd) to determine a background activity of tritium. Females were dosed intraperitoneally with 0.2ml of tritiated water (15.21MBqml-1) on day 14 of lactation. The dose was determined by weighing the syringes before and after the injection (to 0.0001g; Ohaus Analytical Plus). After the isotope had equilibrated with the body water (1h) (Speakman, 1997), an initial blood sample was obtained. A final blood sample was obtained in the same way 24h (±5min) after the initial sample (Speakman and Racey, 1988).
Water was obtained from the blood samples by vacuum distillation (Nagy, 1983) prior to determination of the specific activity of tritium (liquid scintillation counter; Packard, model 1600TR). Samples of 10µl of HTO were weighed (accurate to 0.0001g; Ohaus Analytical Plus) and added to 2ml of scintillation fluid (Ultima Gold XR), vortex-mixed and counted for 5min. To correct for variations in the amount of HTO added, the activity of the samples was expressed per microgram of the original water. Samples were analysed in triplicate, and the mean of two separate counts on each vial was taken. All samples were corrected for background counts from vials containing only scintillation fluid. Specific activity was expressed as disintegrations per minute (disintsmin-1), corrected for quenching.
The fractional turnover rate of tritium (kHTO) over the 24h was calculated using the following equation:
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(Nagy, 1975), where Ci is the specific activity in the initial sample (disintsmin-1µg-1), Cf is the specific activity in the final sample (disintsmin-1µg-1) and t is the time between the initial and final samples (1 day).
Total body water (TBW) (g) was calculated using the following equation:
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where Mi is the mass of the injectate (g) and Cinj is the activity of the injectate solution (disintsmin-1µg-1). The activity of the injectate solution was calculated from the mean of five dilution experiments in which a weighed amount of HTO was added to a known mass of water, and samples of the solution were counted. The activity of the original injectate solution was calculated to be 757,834disintsmin-1µg-1.
To calculate the water turnover in the females (mlH2Oday-1), the fractional turnover rate (kHTO) was multiplied by the total body water (TBW). We assumed that 25% of the water leaving the body was fractionated (Speakman, 1997). We applied a fractionation factor for tritium of 0.9179, assuming a ratio of 3:1 for the equilibrium and kinetic fractionation factors (0.9222 and 0.905, respectively; from Speakman, 1997). One datum was removed from the analysis because the female died during the experiment.
Evaporative water loss was determined by placing individual lactating females (N=10) in a small chamber (308cm3) with a continuous through-flow of air for 1h. Air leaving the chamber was dried (silica gel). The increase in mass of the silica gel was an estimate of the evaporative water loss after correcting for the water content of the air by running the system without a mouse in the chamber for 1h.
Total daily urine and faecal production were measured in five lactating mice. Each female and her litter were placed in a metabolic chamber for 24h with food and water. After 24h, urine was collected and weighed (accurate to 0.0001g; Ohaus Analytical Plus balance), dried to constant mass (60°C, Gallenkamp oven) and reweighed. The estimate of urinary water loss was corrected for evaporation from the sides of the chamber. The water content of fresh faeces was measured by observing mice and collecting faeces within 5s of them being produced. These were then weighed and dried (as above), and the water content was measured. This water content together with the daily production of faeces (dried from the metabolic chamber) were used to calculate daily faecal water loss. The mean total water loss by urinary, faecal and evaporative loss was 30.6±0.8mlday-1 (mean ± S.E.M.). This was subtracted from the water turnover (estimated from tritiated water) to estimate the water diverted to milk production. From the analysis of the composition of milk, 1g of water was equivalent to 1.72g milk. This value was used to convert water in milk production values into total milk production.
Milk quality
Ten of the lactating females used to measure milk production were separated from their pups for a period of approximately 3h on day 15 of lactation. After this separation, which was not long enough to affect milk production (Bateman, 1957; König et al., 1988), the females were injected with 0.25ml of oxytocin to stimulate milk let-down. The teats were manually palpated, and the milk was collected in capillaries. Each teat that was milked was emptied as far as possible because it has been shown that the fat content is atypically low in the first part of the milk extracted (Oftedal, 1984). A total of 0.5ml of milk was collected from each mouse and analysed for water content, fat F, lactose L and protein P content (Rowett Research Institute Analytical Services, Aberdeen, UK). The gross energy content E (kcalg-1; 1cal=4.184J) of the milk was estimated from its composition using the formula developed by Perrin (Perrin, 1958) (cited in Derrickson et al., 1996):
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The units for fat, protein and sugar are grams per gram of whole milk.
Statistical analyses
Means are quoted ± the standard error of the mean (S.E.M.). Repeated-measures analysis of variance (ANOVA) was used to determine the significance of changes in body mass and food intake over time. Least-squares regression analysis was used to examine relationships between maternal food intake, litter size and litter mass. Multiple regression was used to examine the effects of maternal mass, increase in maternal mass and litter size on asymptotic food intake. Direct comparisons of the litter sizes of natural and manipulated females over the same period were made using two-sample t-tests. The significance level for all the above tests was 0.05. All statistical analyses were performed using commercially available software (Minitab versions 7.3 and 11; Ryan et al., 1985).
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Results |
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Food intake increased significantly during the first 13 days of lactation in the control females (F12,910=276.04, P<0.001) from 9.7±0.34g on the day after parturition to 22.4±0.34g on day 12. Over the next 4 days (days 1316), daily food intake remained stable (P=0.263) at an average of 23.1±0.36gday-1 (gross intake 369.5kJday-1). We termed the food intake averaged over these 4 days the asymptotic daily food intake. The food intake of the manipulated females also increased significantly (F10,396=196.9, P<0.001) from 8.1±0.39g on the day after parturition to 19.6±0.55g on day 10 of lactation, thereafter reaching an asymptote until the end of lactation (P=0.608). The asymptotic daily food intake, calculated over the same period as the control mice (days 1316), was 20.8±0.59g (343.2kJ gross energy intake equivalent to 273.3kJ assimilated intake), which was significantly lower than that of the control mice (t=-3.71, d.f.=105, P=0.0005).
There was a significant positive relationship between asymptotic daily food intake I of both the control (r2=0.097, F1,69=7.44, P=0.008) and manipulated (r2=0.205, F1,35=9.00, P=0.005) females and maternal body mass M in late lactation. Daily food intake increased above the asymptotic level on day 18 of lactation (Fig.1B), probably because the pups started to feed directly on the food. On average, the asymptotic daily food intake of the control females at peak lactation was 4.5 times the food intake prior to breeding. The resting metabolic rate of the adult mice at peak lactation was equivalent to 47.05kJday-1 (Johnson et al., 2001) and, hence, at the maximum, sustained gross energy intake (=asymptotic daily food intake multiplied by the energy content of the food) was 8.0xRMR.
Larger litters in the control group were associated with significantly increased asymptotic daily food intake (F10,60=2.42, P=0.017) when litters had fewer than seven pups, but when litters had between seven and 13 pups there was no correlation. The asymptotic daily food intake of mice with 14 pups (26.0±0.70g) was significantly higher than for those with 13 pups (23.5±0.53g) (F1,14=5.79, P=0.029). The asymptotic daily food intake (24.1g) of the single female that raised a natural litter of 15 pups was not significantly different from the intakes of mothers raising either 13 (P=0.79) or 14 (P=0.288) pups. The asymptotic mean intake between litters of 9 and 15 was 22.8gday-1.
On average, the nature of our manipulations meant that there was an over-representation of small and large litters in the manipulated data set (Fig.2). Asymptotic food intake was positively related to litter size for manipulated litters of between three and six pups (F11,25=5.31, P<0.001), but for larger litters there was no further increase in daily food intake with increasing litter size (P=0.381). The difference in mean asymptotic daily food intake between the manipulated and control mice (Fig.1B) therefore reflected in part the over-representation of smaller litters in the manipulated data set. However, this did not explain the entire effect. To establish how the manipulated mice altered their food intake in response to the manipulation, we calculated their expected daily food intake if they had raised the litter to which they had given birth (from the relationship established in the control mice). The difference between their expected and observed intake was calculated and compared with the extent of the manipulation. For those females that were given more pups, there was no significant correlation between the number of pups added and the difference between expected and observed asymptotic daily food intake (P=0.729) (Fig.3). These mice ate significantly less food than expected from the number of pups they gave birth to (t=2.81, d.f.=14, P=0.014), despite the fact their litters were increased. This effect also contributed to the overall lower mean asymptotic daily food intakes of the manipulated individuals. For females that had had the size of their litters reduced, there was a significant positive relationship between the number of pups that had been removed and the difference between actual and expected intake (r2=0.171, F1,21=4.32, P=0.05) (Fig.3). The more pups that were removed from the litter, the less the females ate relative to the amount expected from their litter size at birth. The mothers appeared to be able to downregulate their asymptotic food intake in response to reduction in their litter sizes, but were unable to increase it in response to enlargement of their litters.
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Litter size and mass
The control mice gave birth to an average of 11.7±0.26 pups (range 515) and weaned an average of 11.3±0.24 pups (range 515) (Fig.2). The manipulated litters ranged from 3 to 19 pups at birth and from 3 to 18 pups at weaning (Fig.2). Litter mass in the control group increased from 17.8±0.36g at birth to 86.7±1.41g at weaning. The mean mass of individual pups increased from 1.7±0.14 to 7.9±0.17g over the same time period. Pups from larger litters were significantly smaller than pups from smaller litters in both the control (r2=0.596, F1,69=101.7, P<0.001) and manipulated (r2=0.773, F1,35=119.16, P<0.001) groups (Fig.5). For every increase of one pup in manipulated litter sizes at weaning, there was a decrease in mean pup mass of 0.55g. The same pattern was observed in the control litters, but the trends were not identical. For comparable litter sizes (515 pups), the pups from the manipulated litters were significantly heavier than those from the same-sized control litters (ANOVA F1,90=35.02, P<0.001) (Fig.5).
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Discussion |
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König et al. (König et al., 1988) found that milk production in BALB-c mice, Mus musculus, increased at the start of lactation and then reached a maximum between days 9 and 16, at the same time that we observed a plateau in food intake. Asymptotic daily food intake in the present study was related to the number of pups that were raised up to a litter size of seven, after which there was no further increase in food intake with increasing litter size up to 15 in the unmanipulated litters and up to 18 offspring in the manipulated litters. In contrast, Speakman and McQueenie (Speakman and McQueenie, 1996) found no such limit. However, the absence of an asymptote in this latter study was due to one mouse with a litter size of 13 that ate approximately 40gday-1 in late lactation. This was possibly a mouse that ground its food into the bedding, but was not identified as such in the previous study. Removing this point brings the asymptotic daily food intake down to a value very similar to that observed in the present study.
The apparent asymptote in daily food intake combined with increasing demands of the offspring resulted in the mean mass of pups decreasing with increasing litter size (Fig.5). It is possible that there is a minimum size that a pup must be to survive after weaning which, in combination with the limit on food intake, might place an upper limit on the maximum number of pups raised. There was some evidence supporting the notion that there is a minimum viable pup size since the pups raised in manipulated litters of 1318 were not significantly smaller than the pups from natural litters of 1015 and were heavier than the mass that might be anticipated by extrapolation of the curve relating mean pup mass to litter size in the unmanipulated mice (Fig.5). However, there was no evidence to support the suggestion that limits on sustainable energy intake might set a limit on the maximum number of such minimally sized offspring that a female could raise, since the manipulated females managed successfully to raise these enlarged litters eating slightly, but significantly, less food at peak lactation than their unmanipulated counterparts.
There are several possible reasons why females do not successfully raise more than 15 pups in their first litters, despite being physically capable of successfully raising at least 18 pups. The most likely explanations, however, relate to the impact that performance during the first lactation has on subsequent reproductive events. If these mice are selected to maximise lifetime reproductive output, then we might not necessarily expect them to maximise performance in early breeding attempts if this was detrimental to their subsequent attempts and to overall productivity.
Bateman (Bateman, 1957) calculated an index of regulation (R) that indicates the extent to which females regulate their energy input to the pups:
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where S is the pup mass in large litters, s is the pup mass in small litters, W is the litter mass in large litters and w is the litter mass in small litters. If R=0, then there is no regulation and the mass of litters will be the same regardless of how many pups they contain. If R=1, then there is complete regulation and the individual mass of the pups will be the same regardless of the size of the litter. In the present study, R=0.69 for litters between five and 15, which indicates incomplete regulation, in which the females are investing more to large litters but not sufficient for the pups to be of the same size. This supports the idea that a limit in the system restricts the level of maternal investment. That a limit is present was reinforced by the results from the manipulated litters. Females given more pups to raise did not increase their food intake to accommodate this increased demand. Taking pups away from females resulted in a decrease in their food intake. The more pups that were removed, the greater the decrease. Hence, it appeared that the mice were able to downregulate their food intake, but not to upregulate it. This was also the case in mice of small and large litters made to suckle each others litters towards the end of lactation (Bateman, 1957). The females that originally had large litters rapidly decreased their milk production to the level of small litters, but the mice with small litters failed to increase their milk production when made to suckle a large litter (Bateman, 1957). Although females with reduced litters downregulated their asymptotic daily food intake in late lactation to match that of mothers raising natural litters of the same size, the pups they produced were larger than those in natural litters of the same size (Fig.5). This was probably because it took some time for females to adjust to their smaller litters and, during this phase of adjustment, the small litters were being nourished at the level appropriate for the much larger litters to which the female had given birth.
Although the volume of milk produced was greater in females with heavier litters (Fig.7A), there was a reduction in energy content with increasing volume (Fig.8B). Across the range of 915 pups, the energy provided by the females in milk was not significantly different. Therefore, in addition to there being no increase in maternal food intake across this range of litter size, there was also no increase in milk energy output for the litters. This failure of females to increase production for large litters has been shown previously in mice Mus musculus (Knight et al., 1986; König et al., 1988), rats Rattus norvegicus (Russell, 1980; Fiorotto et al., 1991), cotton rats Sigmodon hispidus (Rogowitz, 1996; Rogowitz, 1998) and dogs Canis familiaris (Meyer et al., 1985). The calculated total daily energy requirement of the litters (expenditure and growth) averaged 63% of the calculated energy supplied to them in milk. This discrepancy reflects the fact that our measurements of respiratory energy expenditure extrapolated up to 24h to yield DEE did not include the costs of activity, and that the milk energy is not completely digested. Since the TER increased in larger litters, but energy transfer in milk to the larger litters was constant, this suggests that larger litters were more efficient in their use of milk energy. The nature of this altered efficiency remains unclear but, given the mean disparity between the input and the estimated requirements, which excluded activity, there was substantial scope for variations in activity between litters of different sizes that would contribute to the efficiency difference.
Although this study indicates that a limit is present in late lactation, it is not clear exactly where this limit is imposed. When females raised large litters, they did not increase their food intake in late lactation to match the increased demand, which suggests that the gut could be limiting. This is supported by the observed asymptote in food intake towards the end of lactation even though the TER of the pups was still increasing at this time. However, the asymptotic food intake could be a consequence of the mammary tissue being limited in its capacity to produce milk, and females may therefore have adjusted their food intake to match milk energy production. Milk output by the mother did not increase with increasing litter size, but rather larger litters received approximately the same as smaller litters. The females appeared to be capable of altering the energy content of the milk by changing its composition, yet when raising more pups they did not increase the energy content.
There are two possible explanations for this failure to adjust the energy content of milk when raising larger litters. The first is that the mammary glands were working at their limit and, although the females appeared to be capable of altering the energy content, they may have been operating at their maximum capacity and were only able to alter the total energy content by decreasing the water content. A second possibility is that the mammary glands were not working at their limit, but were responding to the suckling stimulus received from the pups. Female mice have 10 teats and, assuming that whenever the litter is suckling all the teats are occupied, then the females would receive the same stimulus from a litter of 10 as they would from a litter of 15. This also assumes that litters differing in size were also suckling for the same total duration, but this was not measured. Instead of being limited by the capacity of the mammary glands themselves, the mothers may be limited by the action of hormones such as prolactin and growth hormone. These are released from the anterior pituitary in response to the suckling stimulus and act by stimulating milk synthesis in the mammary glands (Mepham, 1976; Flint and Gardner, 1994; Shand et al., 1995; Travers et al., 1996).
In summary, lactating MF1 mice reached a plateau in food intake at around 23.1gday-1 between days 13 and 16 and with litter sizes of 915. When litter sizes were manipulated, females receiving fewer pups decreased their food intake; however, when pups were added, there was no increase in maternal food intake. Females with larger litters produced more milk but of lower energy content and, thus, milk energy output was not related to litter size.
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Acknowledgments |
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