Nutrient balancing in grasshoppers: behavioural and physiological correlates of dietary breadth
1 Department of Zoology, University of Oxford, South Parks Road, Oxford OX1
3PS, UK
2 University Museum of Natural History, University of Oxford, South Parks
Road, Oxford OX1 3PS, UK
* Author for correspondence (e-mail: david.raubenheimer{at}zoo.ox.ac.uk)
Accepted 26 February 2003
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Summary |
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Key words: nutrient balancing, Locusta migratoria, Schistocerca gregaria, locust, dietary range, herbivore nutrition, macronutrient
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Introduction |
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The most extensively researched group of chemicals that have been studied
in this context are the non-nutrient allelochemicals
(Ehrlich and Raven, 1964;
Rosenthal and Berenbaum, 1992
;
Farrell and Mitter, 1998
;
Berenbaum, 2001
;
Mauricio, 2001
). Surprisingly
little information exists, by contrast, on the role of nutrients in host
selection and the evolution of host range in herbivorous insects
despite the selfevident truth that in most instances nutrition is the
raison d'être for the association between a phytophagous insect
and its host plants. The expectation that nutrient content might be an
important factor in the patterns of host selection by phytophagous insects is
reinforced by the knowledge that great variation exists in the nutrient
content of plants, both in space and time
(Osier and Lindroth, 2001
;
von Fircks et al., 2001
;
Lindroth et al., 2002
;
Gusewell and Koerselman, 2002
;
Oleksyn et al., 2002
), and
that insects are susceptible to such variation
(Scriber and Slansky, 1981
;
Slansky and Rodriguez, 1987
;
Bernays and Chapman, 1994
;
Raubenheimer and Simpson,
1997
; Schoonhoven et al.,
1998
). It has also been suggested that the patterns of host
selection in phytophagous insects might have influenced the macronutrient
content of their plants, in a process analogous to coevolution of insects with
defensive plant-produced allelochemicals
(Moran and Hamilton, 1980
;
Lundberg and Astrom, 1990
;
Augner, 1995
;
Berenbaum, 1995
).
One component of nutritional variability that might play a role is the
concentration of nutrients in relation to nonutilisable bulk such as cellulose
(Abe and Higashi, 1991;
Hochuli, 1996
). It has been
reported that herbivores sometimes avoid plant parts that contain a high
proportion of structural compounds (Choong
et al., 1992
; Williams et al.,
1998
), but the interpretation of this remains unclear because, in
addition to affecting nutrient concentration, structural compounds influence
leaf toughness (Sands and Brancatini,
1991
; Choong et al.,
1992
; Hochuli,
1996
). Furthermore, experiments that separate out the mechanical
from the dilution effects of plant bulk components using artificial diets have
demonstrated that herbivorous insects have a well-developed capacity to
compensate for nutrient dilution by increasing the amount of food processed
(Simpson and Simpson, 1990
;
Raubenheimer and Simpson,
1993
), and the same has been demonstrated using real plant tissue
(Slansky and Feeny, 1977
;
Simpson and Simpson, 1990
).
Plants might also be qualitatively deficient relative to an insect's
nutritional requirements, such that one or more essential nutrients is lacking
or present in a nonutilizable form. For example, insects lack the ability to
synthesise sterols, and some plants contain sterols only in a form that cannot
be utilised by insects (Behmer and
Grebenok, 1998
; Behmer and
Elias, 1999
).
The component of plant variation that, until recently, has received very
little attention in relation to host range in herbivorous insects is the
balance of macronutrients. This is notwithstanding the existence of good
reasons for suspecting an important role for macronutrient balance.
Comparative analysis has revealed, for example, that insects differ widely in
the balance of protein and digestible carbohydrate that gives optimal
performance (Simpson and Raubenheimer,
1993), and fitness costs can be pronounced for insects feeding on
foods that diverge from the required balance (e.g.
Slansky and Feeny, 1977
;
Raubenheimer and Simpson,
1997
; Joern and Behmer,
1997
). Unlike nutrient dilution
(Simpson and Simpson, 1990
),
nutritional imbalance cannot easily be compensated for, because any increased
consumption of the deficient nutrient(s) in an imbalanced food entails
ingesting excesses of others, and existing data suggest that many animals have
a limited capacity to ingest nutrient excesses
(Raubenheimer, 1992
;
Raubenheimer and Simpson,
1997
,
1999
). Unsurprisingly,
therefore, feeding on nutritionally imbalanced foods can have fitness costs
for insects that are avoided when feeding on balanced but nutritionally dilute
foods (Raubenheimer and Simpson,
1993
,
1997
). An animal can, however,
utilise imbalanced foods by incorporating them into a broader diet together
with other foods that contain complementary nutrient imbalances
(Rapport, 1980
;
Chambers et al., 1995
;
Simpson and Raubenheimer,
1995
; Raubenheimer and
Simpson, 1997
).
From the viewpoint of macronutrient balance there are thus grounds to
suspect that there may be two nutritional strategies that represent extremes
in a continuum in host range selection: specialists, which feed on a narrow
range of tissues that closely approximate the required balance of
macronutrients, and generalists, which compose a diet from a wider range of
nutritionally complementary foods. Alternatively, it might be that insects
that are food plant generalists are in fact nutrient specialists, in
that a wide host range better enables them to defend a balanced diet than
plant specialists whose nutrient intake is more vulnerable to variation in a
narrow range of foods (Raubenheimer and
Simpson, 1999). In either event, the ability to tolerate a
sub-optimal balance of ingested nutrients would require appropriate
post-ingestive regulatory responses, such as an ability to selectively excrete
or store ingested excesses. Unfortunately, these relationships remain obscure,
owing to a lack of data relating host range in herbivorous insects to
macronutrient intake and post-ingestive regulatory responses.
We have recently initiated a programme to explore these issues by comparing
in closely related pairs of generalist- and specialist-feeding insects the
diet selection and ingestive, post-ingestive and performance-related responses
to macronutrient imbalance. Previously, we have compared the solitarious and
gregarious phenotypes of the desert locust, which are genetically identical
but, due to their differing ecological circumstances, are likely to encounter
a different range of host plants (Simpson
et al., 2002). We found that the two morphs have similar optimum
macronutrient requirements but that they respond very differently when
confined to nutritionally imbalanced foods. Specifically, the gregarious
morph, which is highly mobile and has a broader host range than the more
sessile solitarious form, ingests greater excesses of the surplus nutrient in
imbalanced foods. These data support the hypothesis that plant generalists are
opportunistic in acquiring nutrient excesses when available and use them to
complement imbalances that might exist in foods that are subsequently
encountered (Raubenheimer and Simpson,
1999
; Simpson et al.,
2002
). Here, we performed a detailed comparison of the ingestive,
post-ingestive and developmental responses of the gregarious form of two
species of grasshopper that differ in their host range: the generalist-feeding
Schistocerca gregaria and the grass-specialist Locusta
migratoria.
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Materials and methods |
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Diets
Locusts were allocated to one of six diet treatments. Six of these
comprised a single food, varying in the ratio of protein to digestible
carbohydrate as follows: 7% protein with 35% digestible carbohydrate (7:35),
14:28, 21:21, 28:14, 35:7 and 42:0. The remaining treatment was given two
nutritionally complementary foods (28:14 and 14:28) simultaneously, and so
allowed to compose a diet of prefered protein:carbohydrate balance. The dry,
granular, synthetic foods were based on those described by Simpson and
Abisgold (1985). All foods
contained 54% cellulose powder and 4% essential micro-nutrients (salts,
vitamins, cholesterol and linoleic acid). Digestible carbohydrate consisted of
a 1:1 mix of sucrose and white dextrin, while the protein contained 3:1:1
casein/peptone/albumen.
Protocol
Representatives of all treatments were run concurrently, with the
experiment being replicated twice to yield a total of 10 locusts per
treatment. Dry mass of food consumed (mass change in the food dishes) was
recorded over the first 3 days, 5 days and until adult ecdysis. From this, the
amounts of protein and carbohydrate consumed could be calculated.
Additionally, the duration of the 5th stadium was recorded to the nearest day.
Upon moulting to adults, the insects were frozen and dried to constant mass in
a desiccating oven at 40°C. Carcasses were weighed to the nearest 0.1 mg
and then lipid-extracted in three 24-h changes of chloroform before being
re-dried and re-weighed to give lipid content. The lipidfree carcasses were
then analysed for nitrogen content using the micro-Kjeldahl procedure as in
Simpson et al. (2002).
Statistical analysis
Unless otherwise stated, data analysis was undertaken using the General
Linear Model facility in SPSS (version 9.0). Details of models and
transformations are provided in the relevant sections of the Results. Rates
and efficiencies were analysed by combining analysis of covariance (ANCOVA)
and graphical analysis, to avoid the statistical and interpretive problems
associated with ratio-based nutritional indices (Raubenheimer and Simpson,
1992,
1994
;
Raubenheimer, 1995
).
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Results |
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Nutrient intake
Fig. 1 shows the protein and
carbohydrate intake selected by Locusta and Schistocerca
over the first 3 days and 5 days of the 5th larval stadium and across the
entire stadium; statistical analyses are presented in
Table 1. Nutrient consumption
by the two species was indistinguishable on day 3 but thereafter progressively
diverged, with the result that, across the stadium, Schistocerca had
selected an intake point significantly higher in protein, but not
carbohydrate, than had Locusta. The greater protein intake by
Schistocerca could not be accounted for by differences in stadium
duration, as the species term remained significant when stadium duration was
entered into the model as a covariate
(Table 1). There were no
significant species x sex interactions.
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Body composition and retention efficiencies
Schistocerca had significantly greater dry body mass than
Locusta (mean ± S.E.M., 331±14.0 mg vs
263±11.6 mg; see Table 2
for statistical comparisons), with no significant species x sex
interaction. Similarly, body nitrogen was higher in Schistocerca
(36.6±1.81 mg) than in Locusta (31.2±1.50 mg), again
with no significant interaction term.
|
To test whether the difference in carcass nitrogen was due to differences in consumption or processing efficiencies, protein intake was entered as a covariate into the model (Table 2). Not surprisingly, body nitrogen was strongly related to protein intake. Additionally, the main effect of species remained significant once protein intake had been taken into account, suggesting that the species differed in the efficiency of nitrogen utilisation. Fig. 2A shows that Locusta retained ingested nitrogen with greater efficiency than did Schistocerca (marginal means ± S.E.M., 34.4±0.468 mg for Locusta and 31.2±0.633 mg for Schistocerca).
|
There were no significant differences between the two species in body lipid content, either as a main effect or in interaction with sex (Table 2).
In addition to nitrogen and lipid, we analysed the component of body mass that was not due to nitrogen or lipid, calculated as: total dry body mass (lipid + nitrogen). This unaccounted mass was significantly greater for Schistocerca (243.1±22.41 mg) than for Locusta (191.2±9.90 mg), with no significant species x sex interaction (Table 2). ANCOVA revealed that this component of body mass was strongly related to protein intake (Fig. 2B) but not to carbohydrate intake, with no residual sex or species difference (Table 2).
To test for concentration differences in body nitrogen, an ANCOVA was performed using body nitrogen as dependent variable and nitrogen-free carcass mass as covariate (Table 3). Carcass mass correlated strongly with carcass nitrogen content but there was no residual species effect. This suggests that the significant species effect in the analysis of variance (ANOVA) of carcass nitrogen (above) is due to the larger overall mass of Schistocerca compared with Locusta rather than a higher concentration of nitrogen.
|
However, a more detailed picture can be obtained by analysing the relationship between nitrogen content and individual components of body mass. There was no significant effect of carcass lipid content as a covariate on carcass nitrogen, and species remained significant in this model (Table 3). There was, however, a strongly significant correlation between unaccounted body mass and carcass nitrogen, but the species term remained significant suggesting that unaccounted body mass alone could not explain differences in carcass nitrogen. Fig. 2C shows that the basis for this effect was a lower nitrogen content per unit of unaccounted body mass in the tissues of Schistocerca (marginal means ± S.E.M., 31.1±0.95 mg) than of Locusta (34.3±0.69 mg). Therefore, whereas Schistocerca had higher levels of nitrogen in the carcass, the concentration of nitrogen in the tissues per unit of unaccounted body mass was lower than in Locusta.
While we did not directly characterise the unaccounted portion of body
mass, its strong dependence on protein intake (above) suggests that it may
consist largely of the non-nitrogen component of amino acids. This is borne
out by the fact that the observed ratios of unaccounted body mass to N for
both species were very similar to the generalised value of 6.25 for
non-nitrogen components of protein:nitrogen
(Long, 1971). Indeed, for
Locusta, the value was statistically indistinguishable from the
expected value (6.21±0.12; P=0.49, N=10; two-tailed
one-sample t-test), while for Schistocerca the value was
slightly but significantly higher (i.e. the proportion of nitrogen was lower)
than expected (6.80±0.12; P=0.003, N=10).
Imbalanced foods
Stadium duration
Stadium duration increased with dietary imbalance in both species, and
Schistocerca experienced slower development on most diets compared
with Locusta (Fig. 3).
A significant diet x species interaction
(Table 4) suggested that the
response to dietary imbalance differed between the species. From
Fig. 3, it can be seen that the
basis for this interaction was, firstly, a shift in the response curve of
Schistocerca to the right, such that in this species the most rapid
development was observed on higher protein diets compared with
Locusta. Secondly, Locusta experienced a disproportionately
large increase in stadium duration on diet 42:0. Means in the figure give the
impression that, conversely, Schistocerca experienced a
disproportionate increase in stadium duration on diet 7:35. This was, however,
not the case, as the mean stadium duration for Schistocerca on this
diet was heavily influenced by a single animal with a stadium duration of 33
days, compared with a mean of 21 days for the remainder of animals in this
group (the cause of the inflated standard error for this group). Excluding
diet 7:35 normalised variances, enabling analysis of untransformed data, and
in fact increased the strength of the diet x species interaction term
(Table 4). This demonstrates
that the main contribution to the analysis of the data for
Schistocerca on diet 7:35 was the large variance rather than the high
mean.
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Across the full stadium, the relationship between diet and the intake of
protein and carbohydrate could be linearised by transforming these variables.
This enabled us to analyse the data using ANCOVA with diet category as
covariate, species and sex as factors and protein or carbohydrate intake as
response variables. For both nutrients, the response variable was
loge-transformed. The covariate was calculated as follows:
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The significant diet x species interactions in these analyses (Table 5) demonstrated that nutrient intake on excess-protein foods, but not excess-carbohydrate foods, was more strongly restricted for Locusta than for Schistocerca (Fig. 4C). The species differences were not due to differences in stadium duration, as they were also apparent for measures taken within a fixed experimental period (i.e. days 3 and 5; see above and also Fig. 4A,B). This suggests that differences in the rate of nutrient intake were involved.
|
Body composition
There was a significant diet x species interaction in the analysis of
dry carcass mass, suggesting that the growth response of Schistocerca
and Locusta to imbalanced foods differed
(Table 6). From
Fig. 5A it can be seen,
firstly, that on excess protein foods growth was reduced in Locusta
but not in Schistocerca. This effect was partly due to nitrogen
(Fig. 5B) and the unaccounted
constituent of body composition (Fig.
5D), but was mainly (in terms of percentage difference) due to
carcass lipid content. Fig. 5C
shows that for foods containing an excess of protein, carcass lipid content in
Locusta dropped monotonically with increasing dietary protein. By
contrast, in Schistocerca, carcass lipids stabilised at a level
marginally below that observed for the self-selecting animals, and this level
was maintained even on diet 42:0, which contained no digestible carbohydrates.
It is worth reiterating at this point that the diets contained only trace
amounts of lipid, and body lipid can therefore only have been derived from
ingested carbohydrate or protein.
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A second notable aspect of the pattern of carcass mass attained by the two species across foods (Fig. 5A) is that Schistocerca was appreciably heavier than Locusta on diet 7:35. This difference was not due to greater lipid stores (in fact, on this food Locusta had larger lipid stores than Schistocerca; Fig. 5C) but was apparent both for carcass nitrogen and, particularly, unaccounted body mass (Fig. 5D). The implication is that Schistocerca was able to allocate higher levels of protein to carcass growth than was Locusta when fed protein-deficient foods.
Retention efficiencies
An ANCOVA was used to test for the effects of diet on the efficiency with
which ingested nitrogen was retained by the two species, with protein intake
as covariate, and species, diet and sex as factors
(Table 6). The fact that the
diet x species interaction observed in the ANOVA on body nitrogen
remained significant in the ANCOVA suggests that the pattern of nitrogen
utilisation efficiencies across the diets differed between the species. The
marginal means for this analysis show that Locusta converted ingested
nitrogen with greater efficiency than did Schistocerca on all diets
except 7:35, where the pattern was reversed
(Fig. 6A).
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To test whether carcass lipid content was related to differences in nutrient intake or utilisation, a model was run using protein and carbohydrate intake as covariates, and species, diet and sex as factors. A significant diet x species interaction revealed that the pattern of variation across diets differed in the efficiency with which the two species converted ingested nutrient into body lipids (Table 6). The marginal means for this analysis (Fig. 6B) show that Schistocerca had higher retention efficiencies on excess protein diets, while Locusta had higher retention efficiencies on excess carbohydrate diets. Separate analyses for the two categories of diets (excess protein and excess carbohydrate) revealed significant main effects of species (including diets 21:21, 28:14, 35:7 and 42:0, F1,48=10.3, P=0.002; while for diets 7:35 and 14:28, F1,18=5.0, P=0.038). This suggests that the basis for the significant diet x species interaction in the full analysis was a reversal across the species of retention efficiencies depending on which nutrient was excessive in the foods, rather than a difference on one category of diets but not the other.
The relationship between nutrient intake and the unaccounted portion of body mass was tested in an ANCOVA with protein and carbohydrate intake as covariates, and species, diet and sex as factors. As was the case in the self-selected diet, protein but not carbohydrate intake was a significant predictor of the unaccounted portion of body mass (Table 6). However, there remained a residual diet x species interaction, suggesting that the pattern across the diets in efficiency of conversion of ingested nutrients to this component of body mass differed between species. The marginal means for this effect (Fig. 6C) show that conversion efficiency was lower for Locusta than for Schistocerca on the diet containing an extreme excess of carbohydrate (7:35), was similar for the two species on diet 14:28 and then dropped off less rapidly for Locusta than for Schistocerca as the relative amount of protein in the foods increased. On diet 42:0, conversion efficiency was similar for the two species.
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Discussion |
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Selected diet
The pattern of nutrient selection in our two study species was
significantly different, with the specialist grass-feeding Locusta
selecting across the stadium an intake point lower in protein, and P:C ratio,
than that selected by the generalist feeder Schistocerca. There were,
however, strong suggestions that the mass-specific nitrogen requirements for
growth of the two species did not differ, since there was no significant
species effect on carcass nitrogen concentration (carcass nitrogen corrected
for nitrogen-free body mass; Table
1). To sustain similar carcass composition in the face of lower
nitrogen intake, Locusta adopted the complementary strategy of higher
retention efficiency (significant species effect in carcass nitrogen corrected
for protein intake; Table 2; Fig. 2a). Interestingly, the
solitarious phase of Schistocerca uses ingested nitrogen more
efficiently than the gregarious phase tested here, and like Locusta
also has a narrower host range (Simpson et
al., 2002).
As was true for nitrogen, there was no difference in the mass of lipid in the carcasses of the two species; since Schistocerca was larger overall, this suggests that the mass-specific lipid content was lower in this species than in Locusta. Given that the insects in this analysis selected their own nutrient intake, and hence nutrient allocation, one interpretation of these data is that Schistocerca has a lower mass-specific requirement for energy storage than does Locusta. However, the fact that the unaccounted portion of body mass (total mass minus lipid and nitrogen) was greater in Schistocerca casts some doubt on this interpretation. While we did not characterise this component chemically, our analyses demonstrate that it is tightly related to protein intake, with no residual species difference (Fig. 2B; Table 2), and might well be the non-nitrogen component of ingested protein (including reduced carbon). Our data suggest, furthermore, that Schistocerca is capable of using ingested protein in energy metabolism since, unlike Locusta, this species maintained body lipid content on diets containing an excess of protein and a deficit of carbohydrate, including diet 42:0, which contained no extractable carbohydrates. Accessible energy in Schistocerca is therefore higher than is indicated by body lipids alone.
The data thus provide no evidence for tissue-level differences in relative
nitrogen and energy requirements between a grass-specialist and a generalist
that includes in its diet both grasses and forbs but do demonstrate distinct
differences in their strategies for fulfilling these requirements. How can
these differences be related to the nutritional characteristics of the
respective evolutionary environments? There are suggestions that forbs may
contain a higher proportion of nitrogen than do grasses
(Mattson, 1980), and one
possibility is that the higher proportion of protein in the selected diet of
Schistocerca reflects this difference. Comparative analyses at the
family and ordinal level have demonstrated that the protein:carbohydrate ratio
of the target food of insects may reflect gross ecological and life-history
differences such as the possession of nitrogen-upgrading symbionts
(Simpson and Raubenheimer,
1993
), but we are unaware of any equivalent data comparing
selected intakes in taxonomically more similar forb and grass feeders.
Alternatively, the higher level of protein in the selected diet of
Schistocerca could be an indirect consequence of having a broader
host range. While a formal comparison has yet to be made, it seems reasonable
to suspect that generalist feeders would encounter greater qualitative and
quantitative variation in host chemistry than do specialists, and a
heterogeneous diet might select for versatile ways of processing ingested
nutrients. Extreme generalist cockroaches (Periplaneta americana L.
and Blatella germanica L.), for example, are capable of extracting
energy from refractory cellulose polymers
(Mira, 1999; Jones and
Raubenheimer, 2000) and also possess nitrogen-upgrading endosymbionts that
enable the usual insect nitrogenous excretory product, uric acid, to be
re-cycled into utilisable amino acids
(Mullins and Cochran, 1986
).
It is interesting in this regard that Schistocerca, but not
Locusta, was observed in our experiment to utilise ingested protein
both as a source of nitrogen and a source of energy, this difference perhaps
reflecting greater biochemical versatility of the generalist. This ability
could, in turn, place a higher premium for Schistocerca on the
acquisition of the dual-purpose protein, relative to carbohydrate, resulting
in the observed protein-rich selected diet. Although the evidence that
Schistocerca uses protein-derived carbon in energy metabolism comes
from imbalanced (carbohydrate-deficient) foods, our observation that on the
self-selected diet less nitrogen was retained (i.e. more was excreted) per
unit of ingested protein in Schistocerca than in Locusta
(Fig. 2A) suggests that the
same might be true on a balanced diet.
By using a protocol in which protein and carbohydrate can be regulated orthogonally, we have therefore been able to measure the preferred intake points of protein and carbohydrate, their utilisation efficiencies and contributions to body composition in Locusta and Schistocerca. These data provide useful comparisons of the nutritional biology of the two species and generate testable hypotheses about the ecological factors that underlie the observed differences. They also provide a reference point for comparing the responses of these species to nutritionally imbalanced foods.
Imbalanced foods
A clear conclusion of our measures of intake of imbalanced and
complementary foods is that, contrary to the ubiquitous assumption in optimal
foraging theory (OFT; Stephens and Krebs,
1986), locusts showed no evidence of feeding in a way that
maximises energy intake. According to this assumption, in the food-switching
treatment, energy maximizers would feed exclusively on the high-carbohydrate
food; instead, both species selected an intake point between the food rails,
suggesting that the ingestive priority was to balance protein and carbohydrate
intake. In the constrained diet treatments, energy prioritisation for
Locusta would be indicated by a horizontal, linear, intake array that
aligned itself with the carbohydrate co-ordinate of the intake target
(Raubenheimer and Simpson,
1993
; Simpson and
Raubenheimer, 1993
). For Schistocerca, the situation is
more complicated because, as our data have demonstrated, this species is
capable of extracting energy both from dietary carbohydrates and proteins. In
this case, the array indicating energy prioritisation would be a negatively
sloped line with a gradient dependent on the relative energy densities (i.e.
on the coefficient of interchangeability with respect to energy) of the two
nutrient groups, a configuration similar to that observed
(Fig. 4). However, the uneven
performance (e.g. development times; Fig.
3) of Schistocerca across treatments demonstrates that,
even if there was equivalence in terms of energy intake across treatments,
this did not translate into functional equivalence. Both the choice and
no-choice treatments in our experiment thus point to the conclusion that some
currency other than energy is primary for generalist and specialist alike.
More relevant is the complex, multivariate nutritional currency, nutrient
balance. To deal with this quantitatively, a metric is needed that integrates
the animal's requirements for various nutrients and its current status in
relation to those requirements. Our chosen measure is `nutritional error',
which achieves an optimal value of 0 for animals that achieve their target
intake and attains negative values at any point in the nutrient space that is
divergent from this (Raubenheimer and Simpson,
1997,
1999
). A further feature of
this measure is that it is sensitive both to deficits and surpluses of the
various nutrients. Given the fact that many components of the ingesta of
heterotrophs are deleterious both in deficit and in surplus of some optimal
rate of intake (a phenomenon that toxicologists call `hormesis';
Gerber et al., 1999
), this
represents a potentially important development on the `maximisation'
assumption of OFT. We hypothesise that a primary target of selection on the
nutritional biology of animals is the relative weighting that regulatory
systems assign to positive (i.e. excesses) and negative (deficits) errors in
the ingestion of various nutritional and non-nutritional (e.g. plant toxins;
Raubenheimer, 1992
;
Simpson and Raubenheimer,
2001
) food components.
In these terms, the intake array displayed by Schistocerca over days 3 and 5 indicates some coefficient of interchangeability among the errors in nutrient intake rather than in the value to the animal of the nutrients themselves. In the most general case, a linear intake array with negative slope shows that the ratio error P/error C is constant across nutritionally imbalanced foods, and if the linear range spans the target rail then this applies, irrespective of whether the foods contain an excess of P or C. This general case can hence be termed the `fixed proportion' regulatory pattern. In the specific case where the slope of the line is 1, it reduces to the `equal distance rule', where error P/error C=1 (i.e. error P = error C), which in geometrical terms means that, for a given scaling (mass in the present case), the animals feed to the point on the nutritional rail where the distance from the target in one dimension equals the distance from the target in the other dimension. The observed array for Schistocerca over days 3 and 5 was similar to this across all diets, with the exception of the extreme diet 42:0, where the intake point lagged behind the linear array.
The arc-shaped intake array of the grass-feeding specialist
Locusta, by contrast, corresponds with minimising the value of (error
P + error C), which in geometrical terms means feeding to the point on the
nutritional rail where the value of total error incurred (i.e. across both
nutrients) attains the minimum value possible for the food's composition
(Simpson and Raubenheimer,
1995; Raubenheimer and Simpson,
1997
,
1999
). A key contrast between
this, the `closest distance rule', and the equal distance rule is that the
positive errors (excesses of nutrients ingested) are greater in the latter,
and so too is the total amount of nutrient ingested (Raubenheimer and Simpson,
1997
,
1999
;
Simpson and Raubenheimer,
2000
).
The patterns of regulation we observed give rise to the interesting
possibility that the closest distance and equal distance rules are more
broadly associated with specialist and generalist feeders, respectively
(Raubenheimer and Simpson,
1997; Simpson et al.,
2002
). While available data are too few for a formal comparative
analysis, it is suggestive that the same correspondence between host range and
the pattern of nutrient balancing has been observed in the comparison of the
generalist-feeding gregarious phase of Schistocerca gregaria and the
specialist solitarious phase (Simpson et
al., 2002
) and also in a comparison of generalist- and
specialist-feeding caterpillars (Lee et
al., 2002
; K. P. Lee, D. Raubenheimer, S. T. Behmer and S. J.
Simpson, manuscript submitted for publication). But which selective factors
might underlie the association between host range and these regulatory
patterns? There is some intuitive appeal in the notion that specialist
feeders, to the extent that their nutritional environment encompasses a
relatively narrow range of food compositions, might forage in a manner that
reduces or minimises the total nutritional error incurred. By contrast,
generalist feeders encountering a wide range of food compositions might be
selected for opportunistically capitalising on individual nutrients when they
are encountered, even if this means temporarily diverting from a state of
nutritional balance. One reason why generalists should be more robust to such
diversions is that the relative breadth of their diet results in an increased
probability that they will subsequently encounter a food with complementary
imbalance, hence turning two excesses into useful, fitness-enhancing nutriment
(Raubenheimer and Simpson,
1999
; Simpson et al.,
2002
).
The approach that we have taken here is to attempt to correlate the
patterns of macronutrient regulation with the position occupied by animals on
the generalistspecialist continuum of host range. Alternatively, the
pattern of macronutrient regulation might itself be used to define the
nutritional strategies of animals, where an animal is considered a
nutrient (as opposed to food plant) generalist or specialist
according to the magnitude of nutritional errors (in relation to the intake
target) that it tolerates. This enables us to frame the comparative question
differently: to what extent does food generalism correspond with
nutrient generalism? Although the studies to date show good
correspondence, as mentioned in the Introduction there remains every
possibility that some insects might have evolved food plant generalism as a
means of reducing nutritional error; i.e. they are food generalists but
nutrient specialists. Conversely, some insects with restricted host range
might have evolved the capacity to tolerate wide variation in the nutrient
composition of their foods. Such questions identify a need for field studies
of the patterns of host plant selection by herbivores (such as that performed
by Raubenheimer and Bernays,
1993), which also measure the nutritional profiles of the plants
concerned and the patterns of macronutrient regulation by the animals.
Whether food specialist or generalist, it might be expected that nutrient
generalists would be better physiologically adapted for dealing
post-ingestively with ingested excesses than are nutrient specialists. A
likely example of this from our experiments is the observation that
Schistocerca was able to channel excess ingested protein into energy
metabolism, as discussed above. Experiments using 13C stable
isotopes have demonstrated that the tobacco hornworm Manduca sexta is
similarly able to use excess ingested amino acids in energy metabolism when
feeding on nutritionally imbalanced foods
(Thompson, 1998). While
individual hornworm larvae are host-plant specialists rather than generalist
feeders they develop induced feeding preferences for the plant on
which they hatch (del Campo et al.,
2001
) this species may nonetheless encounter high levels
of nutritional variability since adult females lay their eggs on a range of
plant species (de Boer, 1993
;
Mira and Bernays, 2002
). The
ability to use excess ingested protein in energy metabolism doubly reduces
nutritional error by simultaneously decreasing the excess of ingested protein
and reducing the energetic deficit due to restricted carbohydrate intake.
The capability of Schistocerca to deal with excess ingested protein might, on the other hand, be related to the greater nitrogen content in the selected (and ecological) diet of this species rather than its broader dietary range. In this interpretation, the response range to nitrogen of Schistocerca is shifted relative to Locusta, rather than broadened as would be expected if host range were the important factor. While possible, we consider this to be unlikely, since it would predict that Schistocerca should utilise protein less well than Locusta on foods with excess carbohydrate. In fact, Schistocerca showed greater nitrogen-processing efficiency on the most protein-deficient food (7:35) and was capable of maintaining body composition better than Locusta irrespective of the direction of nutrient imbalance. We therefore favour the interpretation that the greater concentration of protein in the selected diet of Schistocerca is itself a component of nutritional flexibility, providing as it does both nitrogen and energy to a physiologically flexible generalist.
In conclusion, this work has revealed some interesting differences in the
patterns of nutrient balancing by a pair of generalist- and specialist-feeding
grasshoppers. It is, of course, the case that dietary range is not all that
differs between these species, and the observed differences could be
associated with other factors. However, the fact that they were in the
anticipated direction of greater behavioural and physiological flexibility in
the generalists, and that similar results have been observed in independent
comparisons of the patterns of intake of other generalist- and
specialist-feeding insects (Simpson et
al., 2002; Lee et al.,
2002
; Lee et al.,
2002
; K. P. Lee, D. Raubenheimer, S. T. Behmer and S. J. Simpson,
manuscript submitted for publication), leads us to believe that macronutrient
balance might have been an important selective factor in herbivorous insects.
There is, at the very least, a strong case for extending this kind of analysis
more broadly.
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References |
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Abe, T. and Higashi, M. (1991). Cellulose centered perspective on terrestrial community structure. Oikos 60,127 -133.
Ananthakrishnan, T. N. (ed.) (2001). Insects and Plant Defence Dynamics. Plymouth: Science Publishers.
Augner, M. (1995). Low nutritive quality as a plant defence: effects of herbivore-mediated interactions. Evol. Ecol. 9,605 -616.
Behmer, S. T. and Elias, D. O. (1999). The nutritional significance of sterol metabolic constraints in the generalist grasshopper Schistocerca americana. J. Insect Physiol. 45,339 -348.[CrossRef][Medline]
Behmer, S. T. and Grebenok, R. J. (1998). Impact of dietary sterols on lifehistory traits of a caterpillar. Phys. Ent. 23,165 -175.[CrossRef]
Berenbaum, M. R. (1995). Turnabout is fair play secondary roles for primary compounds. J. Chem. Ecol. 21,925 -940.
Berenbaum, M. R. (2001). Chemical mediation of coevolution: phylogenetic evidence for Apiaceae and associates. Ann. Missouri Bot. Garden 88, 45-59.
Bernays, E. A. and Chapman, R. F. (1994). Host-plant Selection by Phytophagous Insects. New York: Chapman and Hall.
Bernays, E. A. and Graham, M. (1988). On the evolution of host specificity in phytophagous arthropods. Ecology 69,886 -892.
Chambers, P. G., Simpson, S. J. and Raubenheimer, D. (1995). Behavioural mechanisms of nutrient balancing in Locusta migratoria. Anim. Behav. 50,1513 -1523.[CrossRef]
Choong, M. F., Lucas, P. W., Ong, J. S. Y., Pereira, B., Tan, H. T. W. and Turner, I. M. (1992). Leaf fracture-toughness and sclerophylly their correlations and ecological implications. New Phytol. 121,597 -610.
Courtney, S. (1988). If its not coevolution, it must be predation. Ecology 69,910 -911.
de Boer, G. (1993). Plasticity in food preference and diet-induced differential weighting of chemosensory information in larval Manduca sexta. J. Insect. Physiol. 39, 17-24.
del Campo, M. L., Miles, C. I., Schroeder, F. C., Mueller, C., Booker, R. and Renwick, J. A. (2001). Host recognition by the tobacco hornworm is mediated by a host plant compound. Nature 411,186 -189.[CrossRef][Medline]
Ehrlich, P. R. and Murphy, D. D. (1988). Plant chemistry and host range in insect herbivores. Ecology 69,908 -909.
Ehrlich, P. R. and Raven, P. H. (1964). Butterflies and plants: a study in coevolution. Evolution 18,586 -608.
Farrell, B. D. and Mitter, C. (1998). The timing of insect/plant diversification: might Tetraopes (Coleoptera: Cerambycidae) and Asclepias (Asclepiadaceae) have co-evolved? Biol. J. Linn. Soc. 63,553 -577.[CrossRef]
Gerber, L. M., Williams, G. C. and Gray, S. J. (1999). The nutrient-toxin dosage continuum in human evolution and modern health. Q. Rev. Biol. 74,273 -289.[Medline]
Gusewell, S. and Koerselman, M. (2002). Variation in nitrogen and phosphorus concentrations of wetland plants. Persp. Plant Ecol. Evol. Syst. 5, 37-61.
Hochuli, D. F. (1996). The ecology of plant/insect interactions: implications of digestive strategy for feeding by phytophagous insects. Oikos 75,133 -141.
Joern, A. and Behmer, S. T. (1997). Importance of dietary nitrogen and carbohydrates to survival, growth, and reproduction in adults of the grasshopper Agenetotettix deorum (Orthoptera: Acrididae). Oecologia 112,201 -208.[CrossRef]
Jones, S. and Raubenheimer, D. (2001). Nutrional regulation in nymphs of the German cockroach, Blatella germanica. J. Insect Physiol. 47,1169 -1180.[CrossRef][Medline]
Lee, K. P., Behmer, S. T., Simpson, S. J. and Raubenheimer, D. (2002). A geometric analysis of nutrient regulation in the generalist caterpillar Spodoptera littoralis (Boisduval). J. Insect Physiol. 48,655 -665.[CrossRef][Medline]
Lindroth, R. L., Osier, T. L., Barnhill, H. R. H. and Wood, S. A. (2002). Effects of genotype and nutrient availability on phytochemistry of trembling aspen (Populus tremuloides Michx.) during leaf senescence. Biochem. Syst. Ecol. 30,297 -307.[CrossRef]
Long, C. (1971). Biochemists Handbook. London: E., F. and H. Spon.
Lundberg, P. and Astrom, M. (1990). Low nutritive quality as a defense against optimally foraging herbivores. Am. Nat. 135,547 -562.[CrossRef]
Mattson, W. J. (1980). Herbivory in relation to nitrogen. Annu. Rev. Ecol. Syst. 11,119 -161.[CrossRef]
Mauricio, R. (2001). An ecological genetic approach to the study of coevolution. Am. Zool. 41,916 -927.
Mira, A. (1999). Nutritional and evolutionary studies of the hostendosymbiont relationship in the Blattodea. PhD Thesis. Oxford University, UK.
Mira, A. and Bernays, E. A. (2002). Trade-offs in host use by Manduca sexta: plant characters versus natural enemies. Oikos 97,387 -397.[CrossRef]
Moran, N. and Hamilton, W. D. (1980). Low nutritive quality as a defence against herbivores. J. Theor. Biol. 86,247 -254.
Mullins, D. E. and Cochran, D. G. (1986). Nutritional ecology of cockroaches. In Nutritional Ecology of Insects, Mites, Spiders, and Related Invertebrates (ed. F. Slansky and J. G. Rodriguez), pp. 885-902. New York: Wiley.
Oleksyn, J., Reich, P. B., Zytkowiak, R., Karolewski, P. and Tjoelker, M. G. (2002). Needle nutrients in geographically diverse Pinus sylvestris L. populations. Ann. Forest Sci. 59,1 -18.
Osier, T. L. and Lindroth, R. L. (2001). Effects of genotype, nutrient availability, and defoliation on aspen phytochemistry and insect performance. J. Chem. Ecol. 27,1289 -1313.[CrossRef][Medline]
Rapport, D. J. (1980). Optimal foraging for complementary resources. Am. Nat. 116,324 -346.[CrossRef]
Raubenheimer, D. (1992). Tannic acid, protein, and digestible carbohydrate: dietary imbalance and nutritional compensation in locusts. Ecology 73,1012 -1027.
Raubenheimer, D. (1995). Problems with ratio analysis in nutritional studies. Funct. Ecol. 9, 21-29.
Raubenheimer, D. and Bernays, E. A. (1993). Patterns of feeding in the polyphagous grasshopper Taeniopoda eques: a field study. Anim. Behav. 45,153 -167.[CrossRef]
Raubenheimer, D. and Simpson, S. J. (1990). The effects of simultaneous variation in protein, digestible carbohydrate and tannic acid on the feeding behaviour of larval Locusta migratoria (L.) and Schistocerca gregaria (Forskal). I. Short-term studies. Phys. Ent. 5,219 -223.
Raubenheimer, D. and Simpson, S. J. (1992). Analysis of covariance: an alternative to nutritional indices. Ent. Exp. Appl. 62,221 -231.
Raubenheimer, D. and Simpson, S. J. (1993). The geometry of compensatory feeding in the locust. Anim. Behav. 45,953 -964.[CrossRef]
Raubenheimer, D. and Simpson, S. J. (1994). The analysis of nutrient budgets. Funct. Ecol. 8, 783-791.
Raubenheimer, D. and Simpson, S. J. (1997). Integrative models of nutrient balancing: application to insects and vertebrates. Nutr. Res. Rev. 10,151 -179.
Raubenheimer, D. and Simpson, S. J. (1999). Integrating nutrition: a geometrical approach. Ent. Exp. Appl. 91,67 -82.[CrossRef]
Rausher, M. D. (1988). Is coevolution dead? Ecology 69,898 -901.
Rosenthal, G. R. and Berenbaum, M. R. (ed.) (1992). Herbivores: Their Interaction with Secondary Plant Metabolites. London: Academic Press.
Sands, D. P. A. and Brancatini, V. A. (1991). A portable penetrometer for measuring leaf toughness in insect herbivory studies. Proc. Ent. Soc. Washington 93,786 -788.
Schoonhoven, L. M., Jermy, T. and van Loon, J. J. A. (1998). Insect-plant Biology: from Physiology to Evolution. New York: Chapman and Hall.
Schultz, J. C. (1988). Many factors influence the evolution of herbivore diets, but plant chemistry is central. Ecology 69,896 -897.
Scriber, J. M. and Slansky, F. (1981). The nutritional ecology of immature insects. Annu. Rev. Ent. 26,183 -211.
Simpson, S. J. and Abisgold, J. D. (1985). Compensation by locusts for changes in dietary nutrients: behavioural mechanisms. Phys. Ent. 10,443 -452.
Simpson, S. J. and Raubenheimer, D. (1993). A multi-level analysis of feeding behaviour: the geometry of nutritional decisions. Phil. Trans. Roy. Soc. B 342,381 -402.
Simpson, S. J. and Raubenheimer, D. (1995). The geometric analysis of feeding and nutrition: a user's guide. J. Insect Physiol. 7,545 -553.
Simpson, S. J. and Raubenheimer, D. (2000). The hungry locust. Adv. Stud. Behav. 29, 1-44.
Simpson, S. J. and Raubenheimer, D. (2001). The geometric analysis of nutrient-allelochemical interactions: a case study using locusts. Ecology 82,422 -439.
Simpson, S. J., Raubenheimer, D., Behmer, S. T., Whitworth, A.
and Wright, G. A. (2002). A comparison of nutritional
regulation in solitarious- and gregarious-phase nymphs of the desert locust,
Schistocerca gregaria. J. Exp. Biol.
205,121
-129.
Simpson, S. J. and Simpson, C. L. (1990). The mechanism of nutritional compensation by phytophagous insects. In Insect Plant Interactions, vol.II (ed. E. A. Bernays), pp.111 -160.Boca Raton: CRC Press.
Slansky, F. and Feeny, P. P. (1977). Stabilization of the rate of nitrogen accumulation by larvae of the cabbage butterfly on wild and cultivated food plants. Ecol. Monogr. 47,209 -228.
Slansky, F. and Rodriguez, J. G. (ed.) (1987). Nutritional Ecology of Insects, Mites, and Spiders. New York: Wiley.
Stephens, D. W. and Krebs, J. R. (1986). Foraging Theory. Princeton: Princeton University Press.
Thompson, S. N. (1998). Long-term regulation of glucogenesis by dietary carbohydrate and relevance to blood sugar level in an insect Manduca sexta. Int. J. Biochem. Cell Biol. 30,987 -999.[CrossRef]
von Fircks, Y., Ericsson, T. and Sennerby-Forsse, L. (2001). Seasonal variation of macronutrients in leaves, stems and roots of Salix dasyclados Wimm. grown at two nutrient levels. Biomass Bioenergy 21,321 -334.[CrossRef]
Williams, W. P., Davis, F. M., Buckley, P. M., Hedin, P. A., Baker, G. T. and Luthe, D. S. (1998). Factors associated with resistance to fall armyworm (Lepidoptera: Noctuidae) and southwestern corn borer (Lepidoptera: Crambidae) in corn at different vegetative stages. J. Econ. Ent. 91,1471 -1480.
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