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First published online January 19, 2006
Journal of Experimental Biology 209, 541-548 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02016
Effect of diet quality on carbon and nitrogen turnover and isotopic discrimination in blood of a New World nectarivorous bat
1 Departamento de Zoología, Instituto de Biología, UNAM,
Apartado Postal 70-153, 04510, México, DF, México
2 University of Saskatchewan, Department of Biology, Saskatoon, Saskatchewan
S7N 0W0, Canada
* Author for correspondence at present address: Estación de Biología Chamela, Instituto de Biología, UNAM, Apartado Postal 21, San Patricio, Jalisco, 48980, México (e-mail: gherrera{at}ibiologia.unam.mx)
Accepted 29 November 2005
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) than when they were
fed the soya diet (3.3±0.2). Similarly, bats on the amaranth
diet had higher 13C enrichment (2.0±0.2) than bats
on the soya diet (0.1±0.1). Our results support recent
hypotheses of the effect of nutrition on diet-tissue isotopic discrimination
and turnover rate, and further shows that blood stable isotope analysis is an
adequate approach to track seasonal dietary shifts in wild bats.
Key words: blood, carbon-13, fractionation, nectarivorous bat, Glossophaga soricina, nitrogen-15, stable isotope
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,b;
Hobson et al., 2000). This
approach has been used to track dietary shifts through time, but it relies on
a number of assumptions that have not been experimentally tested in most of
the species involved in field studies
(Gannes et al., 1997). For
example, dietary reconstructions assume that animals are in steady-state
equilibrium with their diet. When animals in the wild switch between
isotopically distinct diets, their tissues are not in equilibrium with the new
diet and it becomes critical to know the time required for the tissue to
reflect its new composition. We examined this issue by estimating the
tissue-specific turnover rate of an element using the isotope as a tracer;
this is particularly important when the study is aimed at determining the
timing of dietary shifts. Field studies that use stable isotopes of carbon and
nitrogen simultaneously usually assume close coupling in the turnover rate of
these elements and, consequently, assume that they provide similar time frames
for dietary reconstruction. Studies with wild animals also assume that the
stable isotope composition of the consumer differs from the composition of its
diet in a predictable way and, with some exceptions (e.g.
Haramis et al., 2001), they
frequently use discrimination factors derived for other taxa. Some of the
experimental studies that test these assumptions show that diet composition
could affect diet-tissue isotopic discrimination and turnover rate
(Haramis et al., 2001;
Pearson et al., 2003). The
effect of diet on isotope discrimination has been documented mostly for
nitrogen and it is described by two contrasting hypothesis: (1) nitrogen
isotopic discrimination will increase as % nitrogen (N) increases and the
carbon to nitrogen (C:N) ratio decreases in diets (`quantity hypothesis';
Pearson et al., 2003), and (2)
nitrogen discrimination will decrease as dietary protein quality increases
(`quality hypothesis'; Roth and Hobson,
2000). A recent meta-analysis supports the quality hypothesis, but
rejects the quantity hypothesis (Robbins
et al., 2005).
The effect of diet on elemental turnover rates has been explored only in a
few studies in which turnover rates were estimated in animals fed different
diets (Haramis et al., 2001;
Pearson et al., 2003). The
assumption that the turnover rates of carbon and nitrogen are closely coupled
has found support in some studies (Haramis
et al., 2001; Bearhop et al.,
2002, Evans Ogden et al.,
2004; MacAvoy et al.,
2005) whereas it has been rejected in others
(Hobson and Bairlein, 2003;
Haramis et al., 2001;
Carleton and Martínez del Rio,
2005).
A good example of the effect of diet composition on isotope discrimination
and turnover rate was recently reported in two species of nectarivorous bats,
Glossophaga soricina and Leptonycteris curasoae
(Voigt et al., 2003;
Voigt and Matt, 2004). These
bats were switched to an extremely low nitrogen diet (0.1%N). The most
interesting finding was that carbon and nitrogen turnover rate estimates in
whole blood were extremely long. Carbon half-life was 113-120 days whereas
nitrogen half life was 274-514 days. These values are much higher than any
other estimate in blood of birds and other small mammals
(Hobson and Clark, 1992,
1993;
Haramis et al., 2001;
Bearhop et al., 2002;
Hobson and Bairlein, 2003;
Pearson et al., 2003;
Evans Ogden et al., 2004;
Carleton and Martínez del Rio,
2005; MacAvoy et al.,
2005), and are comparable only to the values found for carbon in
whole blood of catfish Ictalurus punctatus (180 days;
MacAvoy et al., 2001) and
carbon and nitrogen in long-nosed bandicoots Perameles nasuta
(
90 days; Klaassen et al.,
2004). Nectarivorous bats have high mass-specific metabolic rates
(van Helversen and Reyer, 1984; Winter and van Helversen, 2001) whereas
bandicoots have low metabolic rates
(Klaassen et al., 2004) and
catfish metabolism varies with ambient temperature
(MacAvoy et al., 2001). Slow
carbon turnover rate in bat blood was explained as a result of presumably
long-lived erythrocytes (Voigt et al.,
2003). In the case of nitrogen, slow turnover rates were explained
as the result of the effect of the mixing of internal and external sources of
nitrogen, additional fractionation of nitrogen isotopes and individual
metabolic rates (Voigt and Matt,
2004).
Carbon and nitrogen stable isotope analysis has been relatively recently
incorporated into the battery of tools used for studying feeding ecology of
bats (DesMarais et al., 1980;
Herrera et al., 1993,
1998,
2001a,b,
2002;
Fleming et al., 1993;
Fleming, 1995;
Nassar et al., 2003). Some of
these studies examined whole blood
(Herrera et al.,
2001a,b,
2002) and assumed that
half-life of carbon in bat blood was similar to the value found in avian blood
for individuals of similar body mass (e.g. 12 days;
Hobson and Clark, 1992), that
carbon and nitrogen had similar turnover rates, and that diet-tissue
discrimination values were similar to the average values found in other taxa
(e.g. 3.4 for nitrogen and 1 for carbon). The unexpected
findings of Voigt and his colleagues, however, cast serious doubts on the
appropriate use of the isotopic approach in previous studies with wild bat
populations.
Nectarivorous bats were fed a diet of corn syrup, cane sugar, agave syrup
and Opuntia fruits in previous discrimination and turnover
experiments (Voigt et al.,
2003; Voigt and Matt,
2004). These diets were high in carbohydrates but extremely low in
nitrogen (fruits were the main source of nitrogen and contained 0.7%
nitrogen). In addition to its low nitrogen content, such diets most likely
were deficient in some essential amino acids. Probably as a consequence of
this low quality diet, bats lost an average of 8% of their body mass during
the experiments, suggesting that bats had to mobilize body reserves
(Voigt et al., 2003;
Voigt and Matt, 2004).
Although New World nectarivorous bats are well known to feed on flower nectars
that mainly consist of sugars and small amounts of amino acids
(Baker and Baker, 1982;
von Helversen, 1993;
Winter and von Helversen,
2001), pollen and insects are also part of the diet of G.
soricina, L. curasoae and other species of nectarivorous bats
(Carvalho, 1961;
Alvarez and González,
1969; Howell,
1974; Heithaus et al.,
1975; Lemke, 1984;
Herrera et al., 2001b).
Insects and the pollen of some chiropterophilous plants contain protein in
high amounts and are an adequate source of amino acids
(Howell, 1974;
DeFoliart, 1992). A sugar-rich
but protein-poor diet, as used by Voigt and his colleagues, might not be a
good approximation to the diet of nectarivorous bats in the wild.
Consequently, it is necessary to probe the assumptions of previous bat field
isotopic studies with experimental diets that more closely resemble the
quality of their natural diets.
In this study, we determined the turnover rates and diet-tissue
discrimination factors of carbon and nitrogen in whole blood of the
nectarivorous Pallas' long-tongued bat (G. soricina Pallas) using two
diet-switching experiments. It is difficult to provide nectarivorous bats with
diets that satisfy their nutritional requirements using the items that they
feed on in the wild. For example, a single individual might include pollen
from several species of plants and several species of insects during one daily
foraging event (Heithaus et al.,
1975) and these items are not easily accessible in laboratory
facilities. We switched two groups of bats to synthetic diets with protein
soya isolate or amaranth grains as the main source of protein. These items are
not eaten by nectarivorous bats in the wild but are good sources of protein
and are easily accessed under experimental conditions. Protein in soya isolate
(76%; Carias et al., 1995) and
amaranth grains (75-78%; Yañez et
al., 1994) have similar biological values (the percentage of
absorbed protein that is retained;
Robbins, 1993) to the protein
found in pollen and insects (70%;
Smith and Green, 1987;
DeFoliart, 1992;
Van Tets and Hulbert 1999).
Both diets had higher nitrogen content (soya diet: 2.2%N, C:N=18.8; amaranth
diet: 1.3%N, C:N=30.1) than the diet offered by Voigt and his colleagues and
most likely offered a more balanced source of amino acids. We chose
experimental diets after several trials that showed that bats remained healthy
in the long term.
The purpose of the study was twofold. First, the study was aimed at obtaining turnover rates and discrimination factors for nectarivorous bats on diets with an adequate source of nutrients and that more closely represented the conditions that bats face in the wild. We also tested the relationship between body mass changes and carbon and nitrogen turnover rates. We predicted that turnover rates would be slower in bats that lost more mass. The second aim of the study was to test the effect that diets with similar protein biological value but different nitrogen concentration had on carbon and nitrogen turnover rates, metabolic coupling of carbon and nitrogen and diet-tissue discrimination factors. According to the quality hypothesis, there should no be differences in diet-tissue discrimination in both experimental diets. However, if the predictions of the quantity hypothesis were right, discrimination for nitrogen (and probably carbon too) should be higher in the soya diet. We expected close coupling between nitrogen and carbon metabolism with bats on the soya diet because bats on this diet are able to keep a positive nitrogen balance (L.M.M. and L.G.H., unpublished observations) thus reducing the need to using endogenous sources of this nutrient. Longer nitrogen turnover rates were expected on the amaranth diet than the soya diet if its lower nitrogen content forced bats to use endogenous nitrogen sources. Consequently, we considered that uncoupling of carbon and nitrogen metabolism was more likely to occur in bats on the amaranth diet.
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Experimental protocol
The first group was fed the milk diet, and the second group was fed a
mixture of soy protein extract, cereal, table sugar and banana diluted in
water (`soya diet'; Tables 1
and 2) for an additional 18
months. After this period, bats on the milk diet were switched to the soya
diet, whereas bats on the soya diet were switched to a mixture of amaranth,
sucrose, cereal and banana diluted in water (`amaranth diet'; Tables
1 and
2). Bats were kept on the
experimental diets for 105 days and their body mass was measured every week
with an electronic balance (Ohaus®) to the nearest mg. Each component of
the diet was mixed at the beginning of the study to offer isotopically uniform
diets. In the case of banana, we mixed the estimated mass needed for the whole
experiment and separated portions for each day of the study. Banana portions
were frozen and used as needed.
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We were most concerned with not introducing problems of nutritional quality
during the diet switch and so were constrained in terms of what dietary
options we could consider. Previous studies have used relatively small
isotopic differences (Hobson and Bairlein,
2003; Pearson et al.,
2003) and our diets differed isotopically within this range
(Table 3). Milk and soya diets
differed by 1.3 for 
15N and by 2.3 for
13C, whereas soya and amaranth diets differed by 1.5
for 15N and by 4 for 13C
measurements. Soya and amaranth diets had similar biological value but
differed in nitrogen and carbon content
(Table 3). C:N ratios were the
highest in the amaranth diet followed by milk and soya diets in that
order.
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Blood (50-80 µl) was extracted from the antebrachial vein of the
bats at 0, 2, 4, 8, 21, 35, 48, 62, 77, 90 and 105 days. We stopped blood flow
after collecting the sample by pressing a finger on the punctured point. Arms
were used alternately for sampling. Individual bats were bled either at 2 or 4
days after the beginning the experiment to prevent stressing the bats with
excessive handling. Afterwards, bats were bled weekly or bi-weekly. Blood was
placed in plastic vials with 1 ml of 70% ethanol, dried at 40°C to a
constant weight and kept refrigerated until analysis. Samples of the food
offered were collected throughout the experiment, dried and stored in a
refrigerator (-10°C).
Stable isotope analysis
Stable isotope analyses were conducted at the Soil Science Laboratory at
the University of Saskatchewan, Canada. Dried samples were powdered in a small
mortar and pestle. Samples of about 1 mg were then weighed into tin cups and
combusted in a Robo-PrepTM elemental analyzer (Manchester, UK) at
1200°C. Resultant gases were separated and analyzed in a Europa
20:20TM continuous-flow isotope ratio-mass spectrometer (CFIRMS;
Manchester, UK) for stable-carbon and nitrogen isotope ratios on the same
sample. CFIRMS involved the automated sequential measurement of samples
(unknowns) together with reference material. We used two laboratory standards
(egg albumen) for every five unknowns in sequence. Stable-isotope ratios were
expressed in -notation as parts per thousand () deviations from
the international standards PDB (carbon) and air (nitrogen) according to the
equation:
 | (1) |
where X was 13C or 15N and R was the
corresponding ratio 13C:12C or
15N:14N. Based on several hundred replicates of
laboratory standards, we estimated laboratory measurement error to be
±0.3 and ±0.1 for stable nitrogen and
carbonisotope values, respectively.
Turnover rates and trophic discrimination
We obtained suitable isotopic dietary shifts to allow us to model turnover
rates for both 15N and 13C values. We
fitted the isotopic data to equations of the form:
 | (2) |
using Sigmaplot (Version 5). Here Y(t) is the isotopic value of blood at time t, Ya represents the asymptotic tissue isotope value, a is the absolute difference between the initial and asymptotic condition, b is the turnover rate of carbon or nitrogen in blood, and t is time since diet switching. To calculate the half-life of each element, exponential curves were fitted for each individual. Half-life (t50) was defined as -ln(0.5)/b and individual bat values were averaged for each element in each experiment. Trophic discrimination for carbon- and nitrogen-stable isotopes was estimated for each individual on each diet as the difference between average isotopic values of the diet and the derived asymptotic isotopic values (Ya).
Statistical analysis
We used non-parametric tests to evaluate the relationship between body mass
changes and turnover rate, and to compare turnover rates and enrichment
factors between diets. The level of significance for these tests was adjusted
to 0.025 using Bonferroni correction because two data sets were used for each
individual.
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Turnover rates and trophic discrimination
Nitrogen turnover rates did not differ between diets (Mann-Whitney
U=19, P=0.88) but carbon turnover rate was higher with the
amaranth diet (Mann-Whitney U=0, P=0.003). We estimated a
half-life (mean ± s.d.) of 25.5±4.3 days for
15N values and of 24.2±3.7days for
13C values for the bats switched to the soya diet
(Table 4). In the case of bats
switched to the amaranth diet (Table
5), half life of 15N and 13C
values were 24.9±5.9 and 39.6±6.3 days, respectively. Carbon and
nitrogen turnover rates were not affected by body mass change in any of the
diets (Table 6). For purely
illustrative purposes, we depicted elemental turnover patterns for nitrogen
and carbon by fitting a single decay curve to the means of the combined data
for all individuals for each diet switch
(Fig. 1). The enrichment in
15N between diet and blood was higher when bats were fed the
amaranth diet (4.4±0.2) than when they were fed the soya diet
(3.3±0.2, U=0, P=0.003). Similarly, bats on
the amaranth diet had a higher 13C enrichment
(2±0.2) than bats on the soya diet (0.1±0.1,
U=0, P=0.003).
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;
Voigt and Matt, 2004). Unlike
the work of Voigt and his colleagues
(Voigt et al., 2003;
Voigt and Matt, 2004), we
collected blood from the same individual on the second or the fourth day after
beginning the experiment. It remains to be tested whether this additional
collection of blood increased the rate of synthesis of blood cells. However,
blood volumes were the minimum for analysis and other studies with small birds
have used the same blood sampling protocol
(Hobson and Bairlein, 2003;
Pearson et al., 2003;
Carleton and Martínez del Rio,
2005).
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Faster turnover rates in G. soricina in our study compared to
previous bat studies (Voigt et al.,
2003; Voigt and Matt,
2004) were probably explained by the low-quality diet used in
those previous studies. Bats in the wild complement their nectar diet with
insects and pollen and these items are rich sources of protein
(Howell, 1974;
Smith and Green, 1987;
DeFoliart, 1992;
van Tets and Hulbert, 1999).
Thus, unlike bats fed a nitrogen-poor diet (0.1%N) in the experiment by Voigt
and his colleagues, nectarivorous bats have natural diets that include
protein-rich items. In our study, bats were fed diets with higher nitrogen
content (1.3-2.2%N) and with protein sources of biological values (75-78%)
similar to the protein of insects and pollen (70%).
Half-life estimates of carbon in our study provide a time window of dietary
integration of 48-78 days (e.g. two half-lives;
Hobson and Clark, 1993). In
the case of nitrogen, the time window amounts to 50 days. These estimates
are about twice the values assumed in previous studies that analyzed whole
blood isotope composition of wild bats at different times of the year (e.g. 23
days; Herrera et al.,
2001a,b,
2002) but they suggest that
the blood isotope analysis is an adequate method to track seasonal dietary
changes in these animals. Because we conducted our experiments with groups of
bats restrained to a 0.5 m3 cage, it is probable that our results
underestimated turnover rates in wild animals with potentially higher field
metabolic rates. However, house sparrows Passer domesticus have
similar carbon and nitrogen turnover rates in red blood cells even when their
resting metabolic rate differs by a factor of 2
(Carleton and Martínez del Rio,
2005) and increased metabolism does not necessarily equate with
increased elemental turnover through blood cell replacement.
Turnover rate and body condition
In the present study, the amaranth diet had lower nitrogen content than the
soya diet which probably explains body mass losses of bats on this diet.
However, the poorer body condition of bats at the end of the experiment on the
amaranth diet compared to bats on the soya diet did not affect turnover rate
of nitrogen because Nt50 were not different. In contrast,
turnover rate of carbon was slower in bats on the amaranth diet than on the
soya diet (e.g. Ct50 was 62% higher in the amaranth diet).
Similar to previous findings with G. soricina and L.
curasoae (Voigt et al.,
2003; Voigt and Matt,
2004), carbon and nitrogen turnover rates did not increase with
body mass losses in any of the diets, which indicates that higher
Ct50 in bats on the amaranth diet are not simply a result
of an increasing use of endogenous sources. However, one must be cautious in
the case of the relationship between nitrogen turnover rate and body mass
change on the amaranth diet because of the conservative nature of the
Bonferroni correction. A less conservative method
(Rice, 1989) could lead to a
different conclusion for this.
Coupling between carbon and nitrogen dynamics
When bats were fed the soya diet, there was a close coupling between carbon
and nitrogen turnover rates similar to that reported in other vertebrates
(Haramis et al., 2001;
Bearhop et al., 2002;
Evans Ogden et al., 2004;
MacAvoy et al., 2005). In
contrast to our initial predictions, carbon in the amaranth diet had slower
turnover rates than nitrogen, indicating the effect of decoupling of their
metabolic pathways during blood cell formation. Decoupling of carbon and
nitrogen turnover rates was reported in whole blood of garden warblers
Sylvia borin switched from mealworms to a fruit diet
(Hobson and Bairlein, 2003),
canvasback Aythia valiniseria fed a high carbohydrate diet
(Haramis et al., 2001), and
house sparrows fed a corn diet (Carleton
and Martínez del Rio, 2005). Unlike bats on the amaranth
diet, Nt50 was higher than Ct50 in
these studies. However, in liver of house mouse Mus musculus,
Ct50 was much higher than Nt50,
suggesting that carbon turnover reflected total tissue (e.g. carbohydrates,
lipids, proteins and nucleic acids) turnover whereas nitrogen turnover
reflected primarily protein turnover
(MacAvoy et al., 2005).
Accordingly, Ct50 values in the amaranth diet were
probably a result of carbon turnover of other molecules in addition to
protein. Our results confirmed the assumption in previous studies with wild
bats that carbon and nitrogen have similar turnover rates
(Herrera et al.,
2001a,b) but this
may not be true when diets are deficient in some nutrient (e.g. our amaranth
diet) leading to slower carbon turnover rates.
Isotopic discrimination
Diet-tissue nitrogen enrichment (3.3±0.2) for the soya diet
(2.2±0.5%N) was similar to the average value reported in the literature
for mammals (3.3±1.3;
Robbins et al., 2005) under
different diets (5.3±3.6%N) and to the value found in blood of G.
soricina (3.2±1.3) fed a nectar-pollen diet (1.3%N;
Voigt and Matt, 2004). Our
diet-tissue nitrogen enrichment value was similar to that used in previous
isotopic studies with wild bats (Herrera
et al., 2001a, 2003). However, when bats were fed the amaranth
diet (1.3±0.1%N), nitrogen enrichment was significantly higher
(4.4±0.2). Pearson et al.
(2003) hypothesized that
nitrogen isotopic discrimination increased as %N increased and C:N ratio
decreased in diets (the quantity hypothesis). In contrast, Roth and Hobson
(2000) predicted that nitrogen
isotopic discrimination should decrease as dietary protein quality increases
(the quality hypothesis). Because we used diets with protein of similar
biological value, we did not expect nitrogen isotopic discrimination to differ
between them. On the contrary, we found higher 15N enrichment in
bats fed the diet with lower %N and higher C:N ratio, in contradiction of the
predictions of the quantity hypothesis. Similarly, we found that carbon
isotope discrimination was higher in the amaranth (2.0±0.2)
than in the soya (0.1±0.1) diet. Diet-tissue carbon isotope
discrimination associated with the amaranth diet was similar to the value
reported previously for G. soricina on a nectar-pollen diet
(2.3; Voigt et al.,
2003). As suggested by the pattern found in carbon and nitrogen
turnover in bats on the amaranth diet, a significant portion of carbon
incorporated into blood probably originated from non-protein carbon, thus
leading to higher carbon discrimination factors than the soya diet, in which
most carbon was probably derived from protein metabolism.
In summary, our results showed that diet-tissue fractionation and turnover
rates were influenced by diet quality but not to the extent previously
reported for two species of nectarivorous bats
(Voigt et al., 2003;
Voigt and Matt, 2004). The
assumptions of previous studies with wild bats were supported at least in one
of the diets offered in our study, which indicates that blood stable isotope
analysis is an adequate approach to track seasonal dietary shifts.
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Acknowledgments |
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