Introduction
The large asymmetry between plant and consumer nitrogen (N) contents (1)
has led to the N-limitation hypothesis, which stipulates that in most
terrestrial systems low plant N content generally impairs herbivore
performance (1–3). Indeed, many studies have shown that herbivore
growth, survival, and fitness respond positively to increase N or
protein availability (4–11). Nevertheless a handful of studies have
challenged the universality of the N-limitation hypothesis either by
showing that herbivores can cope with N-deficiency, or that increasing N
inputs actually decreases herbivore performance (12–16). One proposed
mechanism to explain these exceptions is an imbalance of N (or protein)
relative to carbohydrates (15). However, limited studies have tested
this carbohydrate limitation hypothesis in situ in field
settings. We propose that species with high carbohydrate demands (e.g.
self-propelled migratory species) are most likely to be negatively
impacted by high plant N and we tested the carbohydrate limitation
hypothesis in the field using a migratory locust in a West African
agroecosystem.
The importance of macronutrient balance on foraging behavior and
performance has been unequivocally demonstrated in laboratory settings
with artificial diets and a theoretical approach termed the Geometric
Framework (17–20). For herbivores, protein and carbohydrate have been
shown to be key nutrients, as illustrated by the fact that animals have
evolved the capacity to regulate their intake to a specific ratio
(21–23). Despite these advances, the link between macronutrient ratios
selected by herbivores in the laboratory and plant nutritional content
in the field has seldom been explored. Plant C:N ratios are commonly
reported in the literature (1, 24–28) but not plant
protein:carbohydrate ratios (for exceptions see (29, 30)). This is
problematic because while N can be used as a proxy for plant protein
content, the majority of plant carbon is structural (i.e. cellulose or
lignin) and undigestible for most herbivores (31, 32). Furthermore,
despite the demonstrated importance of both nutrients on foraging and
performance, the effect of carbohydrate limitation on herbivore
reproduction has yet to be tested in a field setting.
To test the carbohydrate-limitation hypothesis, we used the grass-feeder
locust Oedaleus senegalensis in an annual cropping system
(millet, Pennisetum glaucum ) and manipulated millet
protein:carbohydrate ratios using N fertilizer. We used a grass-feeder
species because grasses typically rely on physical defenses like silica
(33, 34) and not chemical defenses; so our treatment would affect
nutrients and not secondary compounds. Furthermore, all locust species
undergo long, and energetically costly, migrations fueled by lipid
reserves (Hunter et al., 1981; Weis-Fogh, 1952) that come from
carbohydrate consumption (Simpson et al., 2002). O. senegalensisis no exception and can fly up to 350 km in 24h (38–41).
To our knowledge this is the first study to measure the effect of plant
macronutrient content on insect survival and reproduction in the field
and a key step to linking the Geometric Framework methodology with plant
nutritional landscapes in the field.