|
| |
|
|
|
|
||||
| Home Help Feedback Subscriptions Archive Search Table of Contents | ||||
First published online August 31, 2007
Journal of Experimental Biology 210, 3236-3244 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.008060
The interactive effects of protein quality and macronutrient imbalance on nutrient balancing in an insect herbivore
Program in Entomology, Department of Agricultural Biotechnology, Seoul National University, Seoul 151-921, Republic of Korea
e-mail: kwanglee{at}snu.ac.kr
Accepted 24 June 2007
 |
Summary |
|---|
 TOP Summary IntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Key words: carbohydrate, caterpillar, feeding, food selection, foraging, insect herbivore, macronutrient imbalance, nutrient regulation, performance, protein quality
|
Introduction |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
; Schoonhoven
et al., 1998). Plants vary considerably in the mixture and
concentrations of nutrients. Dietary protein and carbohydrate are the two
macronutrients that have featured most extensively in the literature on
herbivore nutritional ecology, with particular reference to their influences
on performance and food selection (Simpson
and Simpson, 1990; Waldbauer
and Friedman, 1991; Simpson
and Raubenheimer, 1993a). Protein is a source of nitrogen for
growth and maintenance of tissues, production of enzymes, etc., as well as a
source of metabolic energy. Besides being the major source of metabolic
energy, carbohydrate is used for structural purposes (cuticle deposition) as
well as being converted into body lipids and some non-essential amino acids
(O'Brien et al., 2002).
The quantity of dietary protein (or nitrogenous nutrients more generally)
has long been recognized as a limiting factor for herbivore survival, growth
and fecundity (McNeill and Southwood,
1978; Mattson,
1980; Scriber and Slanksy,
1981; White,
1993). However, there is a growing consensus that the nutritional
quality of protein is also of critical importance
(Horie and Watanabe, 1983;
Broadway and Duffey, 1988;
Karowe and Martin, 1989;
Felton, 1996). Protein quality
is primarily the function of amino acid composition
(Lehninger et al., 1993). An
imbalanced amino acid composition is associated with reduced growth
(Briegel, 1985;
Karowe and Martin, 1989). The
quality of plant protein is highly variable among different species
(Yeoh et al., 1992), changes
in response to herbivory (Felton et al.,
1992; Bi et al.,
1994), and may be subject to both environmental and genetic
variation (Felton, 1996). This
variability of plant protein quality is likely to impose selective pressure
shaping the behavioural and physiological adaptations of herbivores, but few
studies have rigorously tested this possibility.
Insect herbivores are well known for their capacity to regulate the intake
of both protein and carbohydrate to a certain amount and mixture, where they
can meet their optimal nutrient requirement
(Chambers et al., 1995;
Simpson and Raubenheimer,
2000; Raubenheimer and
Simpson, 2004). There is evidence that failure to reach this
`intake target' incurs a significant performance cost as a consequence of
eating too much of one nutrient and too little of the other
(Simpson et al., 2004).
However, the question remains unanswered how the protein–carbohydrate
balance interacts with variations in protein quality. Predictions have been
made earlier that any negative impact of low-quality protein on herbivore
performance will be magnified with the limitation of overall protein
availability in the food (Hinks et al.,
1993; Felton,
1996; Anderson et al.,
2004).
The aim of the present study was first to investigate interactive effects
of the ratio of protein to digestible carbohydrate and the quality of protein
in the diet on herbivore feeding behaviour, post-ingestive processing and
performance (e.g. survival, growth and development). Having established the
nature of this potential interaction, the pattern of food selection was
studied to seek evidence for compensatory changes in feeding by herbivores in
response to low-quality protein. While a number of studies have described how
compensation by insect herbivores buffers the effect of nutrient dilution or
imbalance (reviewed in Simpson and
Simpson, 1990; Slansky,
1993), relatively little is known about food choice with regards
to varying protein quality in the diet. It has previously been shown that a
greater quantity of low-quality protein is needed by caterpillars to support
maximal growth than a high-quality protein source
(Bloem and Duffey, 1990). It
is therefore likely that an adaptive response from caterpillars would be to
increase their protein intake when encountering low-quality protein diet, in
an attempt to secure an equivalent performance outcome to that achieved by
eating a high-quality protein source. However, eating more of an imbalanced
protein source to gain limiting amino acids will be associated with eating
more than is required of other amino acids, requiring that these are voided
(Zanotto et al., 1994). All
experiments were conducted using the generalist-feeding caterpillars of
Spodoptera littoralis (Boisduval).
|
Materials and methods |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Synthetic foods
Preparation of synthetic foods was based on the method described in Simpson
and Abisgold (Simpson and Abisgold,
1985). All 20 diets contained a fixed total amount of protein plus
digestible carbohydrate (42% by dry mass), but differed in the ratio of
protein to digestible carbohydrate [35% protein with 7% carbohydrate (35:7),
28:14, 21:21, 14:28 or 7:35] and in protein quality. In each P:C, the protein
content of the control diets was composed of a 3:1:1 mixture of
casein:peptone: albumen [which provides a similar amino acid profile to
seedling wheat (Simpson and Abisgold,
1985)]. The gradient of protein quality was generated by replacing
20%, 50% and 80% (dry mass) of this predominantly casein-based protein mixture
with equivalent amounts of zein. Zein is a maize-derived storage protein that
is considered of low nutritional quality for noctuid caterpillars,
attributable to its deficiency of certain essential amino acids [e.g. lysine
and tryptophan (Broadway and Duffey,
1988; Karowe and Martin,
1989)]. Preliminary bioassay also showed 100% mortality for S.
littoralis larvae on all five P:C diets in which the protein content was
composed entirely of zein (K.P.L., unpublished data). The substitution of zein
for casein-based protein mixture allowed manipulation of the dietary protein
quality without changing the total protein quantity in the diets. Sucrose was
used as the source of digestible carbohydrate in the diets. Diets all included
4% of essential micronutrients (salts, vitamins, cholesterol and linoleic
acid). The remaining portion of the food was 54% of the indigestible bulking
agent, cellulose. The dry, granular diets were presented to the insects
suspended at a 1:6 ratio in 1% agar solution.
Protocol
Two separate experiments were performed. The first was a no-choice feeding
experiment in which the caterpillars were restricted to one of 20 diets. In
the second experiment, they were allowed to self-compose their preferred diet
from one of 16 food pairings. In this choice experiment, one of four
equal-P:C-ratio diets (21:21) that had different protein qualities was paired
with one of four protein-biased diets (35:7) that also varied in their protein
quality. A total of 10 replicates was used per treatment in both
experiments.
Upon moulting to the final stadium (day 0), caterpillars were weighed to
the nearest 0.1 mg (obtaining initial fresh mass), and each was placed into
its own experimental arena, a 9 cm-diameter Petri dish that had five 1
mm-diameter perforations in the upper lid to allow ventilation. During the
experimental period, individual insects received either a single (no-choice)
or two food blocks (choice), that were weighed to the nearest 0.1 mg before
being presented to the caterpillars. The fresh mass of each block ranged
between 1300–2000 mg to ensure that food was never deprived but the
surplus was minimal, thus improving the accuracy of intake estimates
(Schmidt and Reese, 1986).
Once the food and insects were inside, the Petri dishes were sealed with a
strip of ParafilmTM to minimize desiccation of the food block, and
maintained at 27°C under a 12:12 light:dark photoregime. After each 24 h
period, any remaining food was removed from the arena and replaced with a
fresh block. Removed blocks were dried to constant mass at 50°C and
subsequently weighed to the nearest 0.1 mg. This procedure was repeated until
each caterpillar had ceased to feed prior to pupation. Food consumption was
calculated as the difference between the initial dry mass of the food
(estimated from the initial fresh mass of the food using regression equations)
and the final dry mass of the food. The dry mass of food consumed provided a
measure of protein and carbohydrate consumption.
When insects pupated, the duration of their final stadium was recorded to
the nearest day. Pupae were killed by freezing and dried to constant mass in a
desiccating oven at 50°C. Dried carcasses were weighed to the nearest 0.1
mg and lipid-extracted in three, 24 h changes of chloroform before being
re-dried and re-weighed. Lipid content was estimated from their mass change.
This chloroform extraction procedure had earlier been shown to be >98%
efficient, relative to Soxhlet distillation
(Simpson, 1983). The
lipid-free carcasses were then analyzed for nitrogen content using the
micro-Kjeldahl procedure. The starting lipid and nitrogen content of each
caterpillar were estimated from linear regression equations established from a
sample of 20 freshly moulted final-instar larvae. The lipid and nitrogen
growth were calculated by subtracting these starting content from the pupal
content.
Statistical analysis
General linear modeling procedures were used to analyse consumption, pupal
dry mass and growth data. These analyses were undertaken using PROC GLM in SAS
v. 8.2 for Windows (SAS Institute, Cary, NC, USA). Efficiencies of conversion
of ingested nutrient to body growth were investigated using ANCOVA with
nutrient consumption data as covariates, to avoid the statistical and
interpretive problems associated with ratio-based nutrient indices
(Raubenheimer and Simpson,
1992). Prior to these parametric analyses, the data were checked
for normality of residuals and homogeneity of variance using
Kolmogorov–Smirnov and Bartlett's test, respectively. Any effects due to
experiment factors on time data (e.g. stadium duration) were tested using the
accelerated failure-time analysis (PROC LIFEREG using Weibull
distribution).
|
Results |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
24=197.49, P<0.001) and with declining
protein quality ( 22=29.06, P<0.001)
(Fig. 1B). The latter effect
was particularly pronounced when the food was extremely carbohydrate-biased
(7:35 diet), as indicated by a significant interaction term between dietary
P:C ratio and protein quality ( 28=34.01,
P<0.001). Pupal dry mass was significantly affected by P:C ratio
(F4,128=11.67, P<0.001), protein quality
(F2,128=4.71, P=0.011), and the interaction
between the two factors (F8,128=4.08,
P<0.001). The effect of low protein quality was to reduce pupal
mass for insects on the low-P:C diets (14:28 and 7:35) but not for those on
the higher ratios (35:7, 28:14 and 21:21). There was only a marginal covariate
(initial fresh mass) effect on pupal mass (F1,128=3.78,
P=0.054). Fig. 1B,C
shows that caterpillars on the lowest protein quality (80% zein) diets
suffered greatest performance costs (i.e. delayed development and reduced
growth), irrespective of the dietary P:C ratios.
|
Across development, the cumulative consumption of protein and carbohydrate
was significantly affected by dietary P:C ratio, protein quality and the
interaction between the two (Table
1). During a fixed period (for instance, days 0–4)
(Fig. 2B), the configuration of
the intake points connecting the five imbalanced control diets (i.e. intake
array) was negative and linear. This straight line later became steeper as the
insects on the low P:C diets (7:35 and 14:28) continued to feed beyond day 4.
However, most caterpillars on protein-rich diets had completed their feeding
by day 4. Caterpillars on the lowest protein quality diets (80% zein) consumed
considerably less nutrients (Table
1) and fed for a significantly longer period (
23=154.77, P<0.001) than those given diets
with superior protein quality.
|
|
The degree of the reduction in consumption with deteriorating protein quality was greatest when the food was extremely imbalanced in the direction of low P:C ratio (Table 1). This pattern of interaction was clearly illustrated when the nutrient intake was compared across the three levels of protein quality (0%, 20%, and 50% zein) (Fig. 2B). For example, on the two lowest P:C diets, animals consumed fewer nutrients as the protein quality declined moderately (20% and 50% zein) (ANOVA: 14:28 diet, F2,24=4.63, P=0.020; 7:35 diet, F2,26=38.23, P<0.001) while consuming almost identical quantities on the three high P:C diets (35:7 diet, F2,26=0.66, P=0.526; 28:14 diet, F2,26=0.16, P=0.851; 21:21 diet, F2,26=0.70, P=0.505).
Nutrient growth and utilization
Insects gained the least amount of body nitrogen when the quality of
dietary protein was the lowest (Fig.
3A). Due to missing data, the analyses of nutrient growth and
utilization were performed using only three levels of protein quality (0%,
20%, and 50% zein). Nitrogen growth was reduced for caterpillars on the
extremely protein-limiting diet (ANOVA: F4,129=35.43,
P<0.001) but tended to be maintained within the range of
8.0–9.3 mg for those across the other four P:C diets, particularly at
the two highest quality levels (0% and 20% zein)
(Fig. 3A). The effect of
lowered protein quality was to reduce nitrogen growth
(F2,129=24.70, P<0.001). As noted by the
significant interaction between the two main effects
(F8,129=2.28, P=0.026), the magnitude of such
impact depended on P:C, with the most pronounced effect demonstrated on the
extremely protein-deficient diet, where even a slight decrease in protein
quality (from 0% to 20% zein) caused substantial reduction in nitrogen growth
(Fig. 3A).
|
). The rate of nitrogen conversion was the lowest in the
extremely protein-excess 35:7 diet but rose as the P:C ratio decreased
(F4,128=57.00, P<0.001). An effect of varying
protein quality was also apparent (F2,128=103.40,
P<0.001), with the efficiency of nitrogen conversion falling with
declining protein quality. There was a significant effect due to an
interaction between P:C ratio and protein quality
(F8,128=3.10, P=0.003). A significant covariate
effect suggests an increase in body nitrogen with protein consumption
(F1,128=484.80, P<0.001). As illustrated in Fig. 3C, lipid growth increased in proportion to the carbohydrate content of the diet (ANOVA: F4,129=59.07, P<0.001). A significant interaction between the main effects was detected (F8,129=4.86, P<0.001), with the effect of protein quality acting in opposite directions depending on P:C ratio. In the high P:C diets (35:7, 28:14 and 21:21), lipid growth tended to be elevated with a lower quality of protein from 0% to 50% zein. In the lowest P:C diet (7:35), however, lipid growth dropped markedly when protein quality was low, relative to the control diet (0% zein).
Lipid conversion efficiency was investigated using ANCOVA with lipid growth as the response variable and protein and carbohydrate consumption as joint covariates. Results revealed significant effects of both covariates (protein, F1,127=30.20, P<0.001; carbohydrate, F1,127=240.17, P<0.001). The conversion rate of nutrients to body lipid was low in the excessively carbohydrate-rich treatment (7:35) (F4,127=16.85, P<0.001) (Fig. 3D). Lipid utilization increased in response to lowered protein quality across the five P:C diets (F2,127=34.58, P<0.001), and there was no significant effect due to the two-way interaction (F8,127=1.04, P=0.408).
Experiment 2: choice experiment
Performance consequences
All insects survived the experiment, except for two individuals provided
with a food pairing of the two lowest-quality protein diets (80%). The protein
quality of the protein-biased diet (35:7) and of the equal-ratio diet (21:21)
significantly affected the duration of the final stadium (accelerated
failure-time analysis: 23=116.42,
P<0.001 and 23=68.96,
P<0.001, respectively). A significant two-way interaction (
29=119.15, P<0.001) was due to pronounced
prolongation of development observed for caterpillars given a food pairing of
the two lowest-quality protein diets (Fig.
4A). Pupal dry mass was influenced by differing protein qualities
of the two choice diets (ANCOVA with initial fresh mass as covariate: 35:7
diet, F3,141=11.02, P<0.001; 21:21 diet,
F3,141=4.41, P=0.005). The observed pattern of
pupal mass described in Fig. 4B
indicated a significant interaction between the two factors
(F9,141=3.96, P<0.001), as the mass-reducing
effect of low-quality protein in the 21:21 diets became apparent when they
were paired with the poorest protein quality 35:7 diet (80% zein). There was a
significant covariate effect (F1,141=15.47,
P<0.001), suggesting that heavier pupae were developed from
initially heavier larvae.
|
Nutrient consumption
Two aspects of consumption were investigated across the feeding period, one
the radian values of the self-selected P:C ratio and the other the amount of
nutrient consumed. Within each measured time period, the most noticeable
effect on food selection was found in response to variation in protein quality
of the 35:7 diet, such that the self-selected P:C ratio significantly
increased for the insects that were given the two moderate 35:7 diets
(Fig. 5,
Table 2) (1.98:1 and 2.09:1 for
20% and 50% zein, respectively) relative to those provided control (1.74:1)
and lowest protein quality 35:7 diet (1.73:1). This pattern was consistent
irrespective of the protein quality of the 21:21 diets, as indicated by the
non-significant interaction term (Fig.
5, Table 2). The
treatment-related difference in the amount of nutrients eaten was analyzed
using the distance of each intake point from the origin in the
protein–carbohydrate intake space as response variable. During the first
3 days, the nutrient consumption was significantly smaller for caterpillars
presented with the food pairing in which the poorest quality 35:7 diet (80%
zein) was paired with the poorest quality 21:21 diet (80% zein), indicating
the significant interaction between the two factors
(Table 2). When the final
consumption was examined, the only significant effect was due to the
differences in the protein quality of the 35:7 diet, with greater amount of
nutrient consumed by the caterpillars on the two moderate quality high-protein
food.
|
|
|
Discussion |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
;
Karowe and Martin, 1989) and
may incur ecological costs, such as reduced fecundity
(Honek, 1993) and increased
vulnerability to parasites and predators
(Benrey and Denno, 1997). A
moderate decline in protein quality (replacing 20% and 50% casein-based
protein mix with zein) did not produce such a marked performance reduction as
for insects on the lowest protein quality (80% zein), indicating that there is
a value between 50% and 80% zein, beyond which severe growth limitation starts
to occur.
The key finding from the present study is that there was a significant
interactive effect of dietary P:C ratio and protein quality, with the negative
impact of low protein quality being amplified as the P:C ratio in the diet
fell. This finding confirms the prediction that the negative consequences of
eating a protein source imbalanced in amino acid composition will be visible
only when total protein quantity reached a critically limiting level
(Hinks et al., 1993;
Felton, 1996;
Anderson et al., 2004).
Consistent with previous studies (Lee
et al., 2002; Lee et al.,
2004), caterpillars of S. littoralis displayed an intake
array across diets of varying P:C ratio that is typical of generalist-feeders
[for the functional explanations in relation to diet breadth, see Raubenheimer
and Simpson (Raubenheimer and Simpson,
2003; Raubenheimer and
Simpson, 2004)]. Additional to this baseline response, across the
five P:C diets, consumption decreased most markedly for caterpillars presented
with the lowest quality (80% zein) protein diet relative to those given diets
of high protein quality. How poor protein quality reduced herbivore feeding
remains to be elucidated but there is the possibility that mechanisms, such as
associatively learned aversion in combination with direct nutrient feedback on
taste sensitivity, are involved (Simpson
and Raubenheimer, 1993b;
Simpson and Raubenheimer,
2000). Reduced rate of ingestion of food deficient in essential
amino acids has been reported in vertebrates
(Gietzen et al., 1986;
Chui et al., 1987). It has
been proposed that low nutritive quality of plants is one possible measure
offering resistance against herbivory (Feeney, 1976;
Moran and Hamilton, 1980;
Augner, 1995;
Berenbaum, 1995), although few
studies have tested this possibility experimentally. Adaptive responses of
herbivores to low-quality food plants include compensatory increases in food
consumption rate and modification of post-ingestive utilization
(Slansky and Feeny, 1977;
Slansky and Wheeler, 1989;
Simpson and Simpson, 1990;
Wheeler and Slansky, 1991;
Slansky, 1993;
Cruz-rivera and Hay, 2000).
Theoretically, such herbivore responses will reduce the effectiveness of
nutrient-based defenses by plants (Moran
and Hamilton, 1980; Berenbaum,
1995). The present data, however, revealed that, at least under a
restricted feeding regime, there was no evidence for such compensatory
increase in intake for lowered protein quality, indicating that low-quality
protein may act as a defensive plant attribute that would hamper insects from
compensatory feeding. The failure to increase consumption may result from
accumulation of excess amino acids in the haemolymph, resulting in inhibition
of further feeding and thus failure to gain more of limiting amino acids (i.e.
`jamming' of protein appetite systems)
(Simpson and Raubenheimer,
1993b; Zanotto et al.,
1994). Interestingly, the present study showed that the reducing
effect of low-quality protein on feeding interacted significantly with dietary
P:C imbalance, as seen by the fact that the degree of the reduction in
consumption with low protein quality was more apparent in the low P:C
diets.
Excessive protein consumed by caterpillars on the highest P:C diet (35:7)
did not translate into extra nitrogen growth, but was accompanied by a fall in
nitrogen conversion efficiency (Lee et
al., 2002; Lee et al.,
2004). This indicated post-ingestive regulation of nitrogen
growth, which is known to include mechanisms such as high rates of nitrogen
excretion (Zanotto et al.,
1993). It would also seem that the severe carbohydrate deficiency
in the 35:7 diet led to caterpillars maintaining their energy balance
via gluconeogenesis (Thompson and
Redak, 2000).
In addition to its effect on feeding, the declining quality of dietary
protein resulted in reduced utilization efficiency of ingested nitrogen to
body nitrogen. Caterpillars are reported to digest zein less efficiently
compared to other protein sources, because of its deficiency of lysine
(Broadway and Duffey, 1988).
Trypsin is a principal protease in many insects including larval Lepidoptera,
and cleaves peptide linkages specifically at the arginine and lysine residues
(Chapman, 1998). A limited
quantity of lysine is therefore likely to reduce the availability of amino
acids or small peptide components to be transported across the gut membrane
and assimilated into the body (Felton et
al., 1992). Another candidate mechanism that may explain reduced
nitrogen utilization is accelerated uric acid production as a consequence of
an increased rate of catabolism of all but the deficient amino acids in the
nutritionally imbalanced protein source
(Horie and Watanabe, 1983;
Karowe and Martin, 1989). This
will certainly result in reduced level of nitrogen pool incorporated to
nitrogen growth.
Despite not being as apparent as for nitrogen growth, there was an
indication that lipid growth was subject to post-ingestive regulation, with
the lipid utilization efficiency being reduced for caterpillars on the
carbohydrate-excess diet (7:35), as reported previously in locusts
(Zanotto et al., 1993). A
striking aspect of lipid utilization was the elevated conversion rate of
ingested nutrient to lipid growth with lowered protein quality irrespective of
the P:C ratio. Perhaps this elevated lipid deposition derived from the carbon
skeletons from amino acids that were ingested in excess on the imbalanced
protein diets and were deaminated to allow excretion of excess nitrogen
(Lehninger et al., 1993). The
consequence of the increased efficiency of nutrient conversion to lipid was
not always related to increased lipid deposition in caterpillars reared on
zein-containing diets. The increment in lipid growth occurred for those on
protein-rich diets. However, despite the heightened utilization rate, lipid
growth fell with declining protein quality on an extremely protein-limiting
diet, and this was mainly due to reduced intake.
One hypothesis that has occasionally been called upon to explain the
widespread occurrence of diet mixing in herbivores is that mixing results from
the need for balancing the requirement for multiple nutrients
(Westoby, 1978;
Rapport, 1980;
Pennings et al., 1993;
Simpson et al., 2004). On the
basis of the significant two-way interaction between P:C ratio and protein
quality, as demonstrated from the no-choice test (see above), caterpillars
would be predicted to alter their strategy of nutrient complementation to
compensate for the low-quality protein. Results shown from the food choice
experiment were largely consistent with this prediction. Once paired with one
of the two 35:7 diets with intermediate protein quality (20% and 50% zein),
caterpillars selected more protein than carbohydrate compared to the level
selected by the insects given the control 35:7 diet, resulting in an increase
in the selected P:C ratio in the former. This tendency to ingest more
low-quality protein is explicable as caterpillars regulating to compensate for
essential amino acids deficient in the food
(Greenstone, 1979;
Bernays and Woodhead, 1984;
Behmer and Joern, 1993). Eating
more protein or amino acids than required may come at a cost
(Slansky, 1993;
Simpson et al., 2004).
However, the need for acquiring limiting amino acid (e.g. lysine) is likely to
function as a driving force outweighing any metabolic costs associated with
processing excess protein intake. When paired with a 35:7 diet with the most
inferior quality protein (80% zein), the insects did not increase their
self-selected P:C ratio. It would seem that they failed to complement their
extra protein requirement by eating this 35:7 diet that would otherwise cause
deleterious consequences (see above), but instead preferred 21:21 diets that
had a better quality protein (e.g. 0, 20, or 50% zein). Probably as a result
of compensatory feeding, both pupal mass and development time were stabilized
in caterpillars on all food-pairings except for the one that had the two
lowest protein quality choice diets, where caterpillars exhibited reduced body
growth and retarded stadium duration because they consumed considerably less
nutrients relative to those on the other treatments.
The present study has attempted to identify the complex nature of the
interactions between the quantity and quality of nitrogenous nutrients in the
diet of an herbivorous insect. It is evident that the extent to which
herbivore survival, development and growth were limited by an imbalanced amino
acid profile depended on the quantity of protein in relation to other
essential macronutrients (in this case, digestible carbohydrate), and
differences in nutrient intake seemed to be the main cause of such performance
consequences. When presented with varying degrees of protein quality,
caterpillars responded by altering their pattern of food selection, which is
explicable as compensation for changes in protein quality. This suggests that
plant protein quality may play a role in influencing herbivore foraging
strategies, in conjunction with other factors such as plant secondary
compounds, food frequency and distance
(Simpson and Raubenheimer,
2001; Behmer et al.,
2001; Behmer et al.,
2002; Behmer et al.,
2003). Finally, the present study provides evidence that variation
in food protein quality has a significant impact on feeding, post-ingestive
utilization and chemical composition of animals, with implications for
patterns of nutrient transfer across trophic levels in ecosystems
(Anderson et al., 2004;
Raubenheimer et al.,
2005).
|
Acknowledgments |
|---|
|
References |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Anderson, T. R., Boersma, M. and Raubenheimer, D. (2004). Stoichiometery: linking elements to biochemicals. Ecology 85,1193 -1202.[CrossRef]
Augner, M. (1995). Low nutritive quality as a plant defence: effects of herbivore-mediated interactions. Evol. Ecol. 9,605 -616.[CrossRef]
Behmer, S. T. and Joern, A. (1993). Diet choice by a grass-feeding grasshopper based on the need for a limiting nutrient. Funct. Ecol. 7,522 -527.[CrossRef]
Behmer, S. T., Raubenheimer, D. and Simpson, S. J. (2001). Frequency-dependent food selection in locusts: a geometric analysis of the role of nutrient balancing. Anim. Behav. 61,995 -1005.[CrossRef]
Behmer, S. T., Raubenheimer, D. and Simpson, S. J. (2002). Herbivore foraging in chemically heterogeneous environments: nutrients and secondary metabolites. Ecology 83,2489 -2501.
Behmer, S. T., Cox, E., Raubenheimer, D. and Simpson, S. J. (2003). Food distance and its effect on nutrient balancing in a mobile insect herbivore. Anim. Behav. 66,665 -675.[CrossRef]
Benrey, B. and Denno, R. F. (1997). The slow-growth-high-mortality hypothesis: a test using the cabbage butterfly. Ecology 78,987 -999.[CrossRef]
Berenbaum, M. R. (1995). Turnabout is fair play: secondary roles for primary compounds. J. Chem. Ecol. 21,925 -940.[CrossRef]
Bernays, E. A. and Chapman, R. F. (1994). Host-Plant Selection by Phytophagous Insects. New York: Chapman & Hall.
Bernays, E. A. and Woodhead, S. (1984). The need for high levels of phenylalanine in the diet of Schistocerca gregaria nymphs. J. Insect Physiol. 30,489 -493.[CrossRef]
Bi, J. L., Felton, G. W. and Mueller, A. J. (1994). Induced resistance in soybean to Helicoverpa zea: role of plant protein quality. J. Chem. Ecol. 20,183 -198.[CrossRef]
Bloem, K. A. and Duffey, S. S. (1990). Effect of protein type and quantity on growth and development of larval Heliothis zea and Spodoptera exigua and the endoparasitoid Hyposoter exiguae. Entomol. Exp. Appl. 54,141 -148.[CrossRef]
Briegel, H. (1985). Mosquito reproduction: imcomplete utilization of the blood meal protein for oögenesis. J. Insect Physiol. 31,15 -21.[CrossRef]
Broadway, R. M. and Duffey, S. S. (1988). The effect of plant protein quality on insect digestive physiology and the toxicity of plant proteinase inhibitors. J. Insect Physiol. 34,1111 -1117.[CrossRef]
Chambers, P. G., Simpson, S. J. and Raubenheimer, D. (1995). Behavioural mechanisms of nutrient balancing in Locusta migratoria nymphs. Anim. Behav. 50,1513 -1523.[CrossRef]
Chapman, R. F. (1998). The Insects: Structure and Function (4th edn). Cambridge: Cambridge University Press.
Chui, Y. N., Austic, R. E. and Rumsey, G. L. (1987). Interactions among dietary minerals, arginine and lysine in rainbow-trout (Salmo gairdneri). Fish Physiol. Biochem. 4,45 -55.[CrossRef]
Cruz-rivera, E. and Hay, M. E. (2000). Can quantity replace quality? Food choice, compensatory feeding, and fitness of marine mesograzers. Ecology 81,201 -219.
Feeny, P. (1976). Plant apparency and chemical defense. Recent Adv. Phytochem. 10, 1-40.
Felton, G. W. (1996). Nutritive quality of plant protein: sources of variation and insect herbivore responses. Arch. Insect Biochem. Physiol. 32,107 -130.[CrossRef]
Felton, G. W., Donato, K. K., Broadway, R. M. and Duffey, S. S. (1992). Impact of oxidized plant phenolics on the nutritional quality of dietary protein to a noctuid herbivore, Spodoptera exigua. J. Insect Physiol. 38,277 -285.[CrossRef]
Gietzen, D. W., Leung, P. M.-B., Castonguay, T. W., Hartman, W. J. and Rogers, Q. R. (1986). Time course of food intake and plasma and brain amino acid concentrations in rats fed amino acid-imbalanced or -deficient diets. In Interaction of the Chemical Senses with Nutrition (ed. M. R. Kare and J. G. Brand), pp.415 -456. New York: Academic Press.
Greenstone, M. H. (1979). Spider feeding behaviour optimises dietary essential amino acid composition. Nature 282,501 -503.[CrossRef]
Hinks, C. F., Hupka, D. and Olfert, O. (1993). Nutrition and the protein economy in grasshoppers and locusts. Comp. Biochem. Physiol. A 104,133 -142.
Honek, A. (1993). Intraspecific variation in body size and fecundity in insects: a general relationship. Oikos 66,483 -492.[CrossRef]
Horie, Y. and Watanabe, K. (1983). Effect of various kinds of dietary protein and supplementation with limiting amino acids on growth, haemolymph components and uric acid excretion in the silkworm, Bombyx mori. J. Insect Physiol. 29,187 -199.[CrossRef]
Karowe, D. N. and Martin, M. M. (1989). The effects of quantity and quality of diet nitrogen on the growth, efficiency of food utilization, nitrogen budget, and metabolic rate of fifth-instar Spodoptera eridania larvae (Lepidoptera: Noctuidae). J. Insect Physiol. 35,699 -708.[CrossRef]
Lee, K. P., Behmer, S. T., Raubenheimer, D. and Simpson, S. J. (2002). A geometric analysis of nutrient regulation in the generalist caterpillar Spodoptera littoralis (Boisduval). J. Insect Physiol. 48,655 -665.[CrossRef][Medline]
Lee, K. P., Raubenheimer, D. and Simpson, S. J. (2004). The effects of nutritional imbalance on compensatory feeding for cellulose-mediated dietary dilution in a generalist caterpillar. Physiol. Entomol. 29,108 -117.[CrossRef]
Lehninger, A. L., Nelson, D. L. and Cox, M. M. (1993). Principles of Biochemistry (2nd edn). New York: Worth Publishers.
Mattson, W. J. (1980). Herbivory in relation to plant nitrogen content. Annu. Rev. Ecol. Syst. 11,119 -161.[CrossRef]
McNeill, S. and Southwood, T. R. E. (1978). The role of nitrogen in the development of insect/plant relationships. In Biochemical Aspects of Plant and Animal Coevolution (ed. J. Harborne), pp. 77-98. London: Academic Press.
Moran, N. and Hamilton, W. D. (1980). Low nutritive quality as defense against herbivores. J. Theor. Biol. 86,247 -254.[CrossRef]
O'Brien, D. M., Fogel, M. L. and Boggs, C. L.
(2002). Renewable and nonrenewable resources: amino acid turnover
and allocation to reproduction in Lepidoptera. Proc. Natl. Acad.
Sci. USA 99,4413
-4418.
Pennings, S. C., Nadeau, M. T. and Paul, V. J. (1993). Selectivity and growth of the generalist herbivore Dolabella auricularia feeding upon complementary resources. Ecology 74,879 -890.[CrossRef]
Rapport, D. J. (1980). Optimal foraging for complementary resources. Am. Nat. 116,324 -346.[CrossRef]
Raubenheimer, D. and Simpson, S. J. (1992). Analysis of covariance: an alternative to nutritional indices. Entomol. Exp. Appl. 62,221 -231.[CrossRef]
Raubenheimer, D. and Simpson, S. J. (2003).
Nutrient balancing in grasshoppers: behavioural and physiological correlates
of dietary breadth. J. Exp. Biol.
206,1669
-1681.
Raubenheimer, D. and Simpson, S. J. (2004). Organismal stoichiometry: quantifying non-independence among food components. Ecology 85,1203 -1216.[CrossRef]
Raubenheimer, D., Zemke-White, W. L., Phillips, R. J. and Clements, K. D. (2005). Algal macronutrients and food selection by the omnivorous marine fish Girella tricuspidata.Ecology 86,2601 -2610.[CrossRef]
Schmidt, D. J. and Reese, J. C. (1986). Source of error in nutritional index studies of insects on artificial diet. J. Insect Physiol. 32,193 -198.[CrossRef]
Schoonhoven, L. M., Jermy, T. and van Loon, J. J. A. (1998). Insect-Plant Biology: From Physiology to Evolution. London: Chapman & Hall.
Scriber, J. M. and Slansky, F. (1981). The nutritional ecology of immature insects. Annu. Rev. Entomol. 26,183 -211.[CrossRef]
Simpson, S. J. (1983). Changes during the fifth instar of Locusta migratoria in the rate of crop emptying and their relationship to feeding and food utilization. Entomol. Exp. Appl. 33,235 -243.
Simpson, S. J. and Abisgold, J. D. (1985). Compensation by locusts for changes in dietary nutrients: behavioural mechanisms. Physiol. Entomol. 10,443 -452.
Simpson, S. J. and Raubenheimer, D. (1993a). A multi-level analysis of feeding behaviour: the geometry of nutritional decisions. Philos. Trans. R. Soc. Lond. B Biol. Sci. 342,381 -402.[CrossRef]
Simpson, S. J. and Raubenheimer, D. (1993b). The central role of the haemolymph in the regulation of nutrient intake in insects. Physiol. Entomol. 18,395 -403.
Simpson, S. J. and Raubenheimer, D. (2000). The hungry locust. Adv. Study Behav. 29, 1-44.
Simpson, S. J. and Raubenheimer, D. (2001). The geometric analysis of nutrient-allelochemical interactions: a case study using locusts. Ecology 81,422 -439.
Simpson, S. J. and Simpson, C. L. (1990). The mechanisms of nutritional compensation by phytophagous insects. In Insect-Plant Interactions. Vol.II (ed. E. A. Bernays), pp.111 -160. Boca Raton, FL: CRC Press.
Simpson, S. J., Sibly, R. M., Lee, K. P., Behmer, S. T. and Raubenheimer, D. (2004). Optimal foraging when regulating intake of multiple nutrients. Anim. Behav. 68,1299 -1311.[CrossRef]
Slansky, F. (1993). Nutritional ecology: the fundamental quest for nutrients. In Caterpillars: Ecology and Evolutionary Constraints on Foraging (ed. N. Stamp and T. M. Caesy), pp. 29-91. New York: Chapman & Hall.
Slansky, F. and Feeny, P. (1977). Stablization of the rate of nitrogen accumulation by larvae of the cabbage butterfly on wild and cultivated food plants. Ecol. Monogr. 47,207 -228.
Slansky, F. and Wheeler, G. S. (1989). Compensatory increases in food consumption and utilization efficiencies by velvetbean caterpillars mitigate impact of diluted diets on growth. Entomol. Exp. Appl. 51,175 -187.[CrossRef]
Thompson, S. N. and Redak, R. A. (2000). Interactions of dietary protein and carbohydrate determine blood sugar level and regulate nutrient selection in the insect Manduca sexta L. Biochim. Biophy. Acta 1523,91 -102.[Medline]
Waldbauer, G. P. and Friedman, S. (1991). Self-selection of optimal diets by insects. Annu. Rev. Entomol. 36,43 -63.[CrossRef]
Westoby, M. (1978). What are the biological bases of varied diets? Am. Nat. 112,627 -631.[CrossRef]
Wheeler, G. S. and Slansky, F. (1991). Compensatory response of the fall armyworm (Spodoptera frugiperda) when fed water- and cellulose-diluted diets. Physiol. Entomol. 16,361 -374.
White, T. C. R. (1993). The Inadequate Environment: Nitrogen and the Abundance of Animals. New York: Springer.
Yeoh, H.-H., Wee, Y.-C. and Watson, L. (1992). Leaf protein contents and amino acid patterns of dicotyledonous plants. Biochem. Syst. Ecol. 20,657 -663.[CrossRef]
Zanotto, F. P., Simpson, S. J. and Raubenheimer, D. (1993). The regulation of growth by locusts through post-ingestive compensation for variation in the levels of dietary protein and carbohydrate. Physiol. Entomol. 18,425 -434.
Zanotto, F. P., Raubenheimer, D. and Simpson, S. J. (1994). Selective egestion of lysine by locusts fed nutritionally unbalanced foods. J. Insect Physiol. 40,259 -265.[CrossRef]
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
