Frank Slansky

NUTRITIONAL ECOLOGY OF ENDOPARASITIC INSECTS AND THEIR HOSTS: AN OVERVIEW

Abstract The impact of insect endoparasites (parasitoids) on the physiology and behaviour of their hosts is reviewed within the context of the nutritional ecology of the parasitoids and their hosts. Alterations in the consumption, utilization and allocation of food by parasitized hosts are common, as are internal changes in their metabolic physiology. Gregarious parasitoid species frequently increase feeding by their host larvae whereas solitary parasitoid species often reduce feeding and growth of their hosts. Many parasitoid-associated changes in host physiology and behaviour are interpreted to be of adaptive significance to parasitoids. Substantial circumstantial evidence suggests, and a few direct tests of such adaptive significance indicate, that parasitoids alter their hosts in ways beneficial to their own fitness. However, most of the changes in parasitized hosts are of unknown cause and undocumented significance to the parasitoids. Several relevant hypotheses are presented, and these require extensive evaluation (often requiring novel experimental approaches) before a thorough understanding of parasitoid nutritional ecology is established.

Caterpillars' compensatory feeding response to diluted nutrients leads to toxic allelochemical dose

Many herbivores increase their consumption rate as dietary nutrient concentration declines. This compensatory response can mitigate the fitness‐lowering impact of reduced food quality, but little is known about its costs. In this study we tested the hypothesis that one cost to a faster consumption rate can be the ingestion of a toxic dose of an allelochemical occurring in the food. We fed velvetbean caterpillars a diet with progressively diluted nutrient levels but containing the same concentration (% fresh mass, fm) of caffeine, a methylxanthine alkaloid. Larvae compensated for the reduced nutrient level, with those fed the most diluted diet increasing their biomass‐relative consumption rate (fm) 2.6‐fold over larvae fed the undiluted diet. Consequently, their rate of caffeine ingestion increased to a pharmacologically effective dose, interfering with food utilization, slowing growth, reducing subsequent feeding and lowering survival. These results suggest that greater allelochemical ingestion can be one cost of an increased consumption rate, although additional studies with other allelochemicals and species are necessary to more broadly evaluate whether insects can adaptively balance their intake of nutrients and allelochemicals through adjustments in consumption rate. In addition, these results highlight the importance of measuring consumption rates of allelochemicals and other ingested biocides, not just their dietary concentration, when assessing efficacy against herbivores.

Compensatory increases in food consumption and utilization efficiencies by velvetbean caterpillars mitigate impact of diluted diets on growth

Fresh weight (fw) food consumption by caterpillars of Anticarsia gemmatalis Hübner (Lepidoptera: Noctuidae) increased almost 2‐fold as the nutrients in an artificial diet were increasingly diluted with water (diets contained 65, 79, 86 or 89% fw water). Nonetheless, dry weight (dw) relative consumption rate (RCR) declined with diet dilution. The efficiency at which the consumed food is digested and assimilated (approximate digestibility, AD) increased on the 3 diluted diets, and the efficiency at which digested food is converted to biomass (ECD) increased on the 79 and 86% fw diets. As a consequence, dw gained and relative growth rate (RGR), which is the product of RCR × AD × ECD, on the 79% fw diet were similar to those on the 65% fw diet, but they declined on the more diluted diets. Relative nitrogen consumption rate also declined with dietary dilution, but this was compensated by an increase in nitrogen utilization efficiency such that the product of these, relative nitrogen accumulation rate, was similar on all four diets. Insect lipid content declined from 32% on the undiluted diet to 13% dw on the most diluted diet, and was primarily responsible for the decline in RGR. The increases in fw consumption and AD, while not preventing a decline in RGR on the two most diluted diets, mitigated the impact of dietary dilution (e.g., without these increases, RGR on the most diluted diet would have been only 43% of that attained). These results indicate that the consumption and utilization of food are dynamic processes, and that caterpillars of A. gemmatalis, like many other insects, exhibit compensatory responses to changes in dietary quality.

Food consumption and utilization responses to dietary dilution with cellulose and water by velvetbean caterpillars, Anticarsia gemmatalis.

Abstract Dilution of an artificial diet with water or cellulose to nutrient levels of 32% (undiluted), 19% and 10% fresh weight (fw) resulted in increased fw and dry weight (dw) food consumption (both absolute amounts and weight‐relative rates) by velvetbean caterpillars, Anticarsia gemmatalis Hübner. Despite these increases, the absolute amount and relative rate of nutrient intake by the caterpillars declined with dilution, as did their dw gain and dw (% fw) and lipid (% dw) contents. The proportion of consumed food (dw, including cellulose) that was digested and absorbed declined with increased dietary cellulose; however, the proportion of consumed nutrients (dw, excluding cellulose) that was digested and absorbed was not affected by the presence of cellulose, although it increased slightly (but significantly) with dietary water. The efficiency with which the absorbed nutrients were converted to biomass energy showed a negative relationship with the various measures of food consumption and thus a positive relationship with dietary nutrient level.

Food utilization by insects: Interpretation of observed differences between dry weight and energy efficiencies

Over 80% of the values of approximate digestibility (AD), efficiency of conversion of assimilated food to biomass (ECD) and efficiency of conversion of ingested food (ECI) calculated using energy terms are greater than the corresponding dry weight (DW) values, based on data for over 65 species (38 studies; number of comparative values: AD=139, ECD=128 and ECI=169). Largest positive differences (energy>DW values) are 30 (AD, ECD) and 24 (ECI) percentage points and largest negative differences (energyDW efficiency values are commonly expected for AD because of the generally greater energy content of food than feces, and for ECD and ECI because of the generally greater energy content of insect biomass than ingested and assimilated food. Deviations from predicted differences in surveyed literature data are discussed in terms of possible methodological sources of error.

Compensatory responses of the fall armyworm (Spodoptera frugiperda) when fed water‐ and cellulose‐diluted diets

Abstract Caterpillars of the noctuid moth, Spodoptera frugiperda (J. E. Smith), reared on artificial diets diluted with cellulose and water, increased fresh weight (fw) consumption 2.2–2.5‐fold over those on the undiluted diet. At moderate levels of water‐ or cellulose‐dilution, the increased consumption, combined with increased digestion and absorption of nutrients (ADNU), sufficiently compensated for the reduced nutrient intake to achieve pupal biomass equivalent to that of pupae from the undiluted diet. At higher levels of water‐ and cellulose‐dilution, fw consumption and ADNU increased further but pupal dry weight declined on the water‐diluted diets. At each level of dilution fw consumption and ADNU increased similarly on the water‐ and cellulose‐diluted diets, but biomass gain was reduced on the water‐ compared with the cellulose‐diluted diets. This was due in part to lowered food conversion efficiency on the water‐diluted diets, possibly caused by increased costs of metabolizing the wetter diets. Our data support the hypothesis that consumption rates are regulated by a nutrient feedback mechanism. Our data also suggest that digestive enzyme activity is correlated with consumption. Furthermore, the cost of increased consumption rates on diets of reduced energetic value may constitute a substantially greater energy expenditure than previously believed. However, this cost was insufficient to reduce relative growth rates but was apparently manifested in lowered lipid accumulation.

Age‐specific flight behavior in relation to body weight and lipid content of Ips calligraphus reared in slash pine bolts with thick or thin inner bark (phloem)

Rearing larvae of Ips calligraphus (Germar) (Coleoptera: Scolytidae) in bolts of typical slash pine, Pinus elliottii Engelm. var. elliottii, with ‘thin’ (TN; 0.5–1.5 mm) phloem (inner bark) relative to adult beetle body width significantly reduced body weight and lipid content of emerging adults compared with ‘thick’ (TK; 2.5–3.5 mm) phloem‐reared adults. Unmated (pre‐nuptial) TK beetles averaged 2‐fold longer daily and lifetime flight duration than TN beetles. Daily flights were highly variable, averaging < 20 min (longest daily flight = 173 min). TK and TN beetles initiated flight, and the greatest number flew, on the first or second day after emergence from their rearing bolt % of beetles flying and survival gradually declined to zero by day 9. Males (both TK and TN) averaged 2.5 days of flight, ca. 1 day longer than females. Fliers lived ca. 2‐fold longer than non‐fliers. Among TK and TN fliers, significant but weak positive correlations occurred between body weight and lifetime flight duration. Poor correlation between lifetime flight duration and longevity suggests little physiological cost to flight, but effects on fecundity were not assessed. Flight by mated, egg‐laying (post‐nuptial) beetles was substantially delayed (peaking on day 6), suggesting degeneration and subsequent regeneration of flight muscles.

Interactions of allelochemicals with dietary constituents: effects on deterrency

Abstract. That variation in the water and nutrient content of plant tissues affects allelochemical toxicity to insects is well established. However, little is known about how these dietary constituents influence allelochemical deterrency. In vertebrates, deterrency of particular allelochemicals increases with dietary water, and decreases with an increase in dietary nutrients. We determined if these findings were relevant to phytophagous insects through an experimental design that allowed us to vary independently the content of water (70–90% fresh mass, fm, with nutrient level at 10% fm) and nutrients (10–30% fm with water level at 70% or 80% fm) in an artificial diet through use of alphacel, a non‐nutritive cellulose fibre. We examined the effect of these dietary manipulations on allelochemical deterrency by comparing larval feeding responses of two noctuid species, the oligophagous Anticarsia gemmatalis Hübner and the polyphagous Spodoptera frugiperda (J. E. Smith), to a control diet and an allelochemical‐treated diet in two consecutive, no‐choice tests. These tests were restricted to 3 min to minimize post‐ingestive influences. From an initial twelve compounds tested, all but two were excluded for the following reasons: (i) failure to elicit an intermediate level of deterrency at <1% fm (i.e. albizziin, amygdalin, hordenine, ouabain, pipecolic acid, salicin, sinigrin and umbelliferone); (ii) an apparently rapid toxic effect (nicotine hydrogen tartrate); and (iii) adsorption to alphacel (quinine hydrochloride), which may have reduced deterrency. The deterrency of caffeine and linamarin increased with dietary water but was unaffected by nutrient content for both species. The similar results for an alkaloid and a cyanogenic glycoside, with two species differing considerably in feeding habits, suggest that dietary water is likely to influence the defensive efficacy of a broader range of deterrent allelochemicals to a variety of plant‐feeding insects.

Food consumption, utilization and detoxification enzyme activity of larvae of three polyphagous noctuid moth species when fed the botanical insecticide rotenone

We assessed the effects of the isoflavonoid rotenone, an insecticidal allelochemical occurring in various legumes, on larval performance of three polyphagous noctuid species: the corn earworm (CEW), the fall armyworm (FAW) and the southern armyworm (SAW). As rotenone concentration was increased up to 1% fresh mass in an artificial diet, neither mortality (for all three species) nor food consumption (for SAW and FAW) was significantly affected, but developmental time of the latter two species was prolonged. In contrast, for CEW developmental time was shortened and food consumption declined, especially at the two highest rotenone concentrations. Final biomass of all three species declined as dietary rotenone increased.

Lipid content and fatty acid composition of larvae and adults of the velvetbean caterpillar, Anticarsia gemmatalis, as affected by larval diet

Eight fatty acids were found in the food, larvae and adults of the velvetbean caterpillar, Anticarsia gemmatalis, with C16:0, C18:0, C18:1, C18:2 and C18:3 accounting for over 90% of the total. Fatty acid composition of the larvae tended to reflect that of their food. The most striking differences were the high percentages of C18:1 and C18:2 and the low percentage of C18:3 in the artificial diet and artificial diet-reared larvae compared to the foliage of three species of legume food plants (soybean, Glycine max; pigeon pea, Cajanus cajan; and hairy indigo, Indigofera hirsuta) and foliage-reared larvae. Lipid content (%dw) declined during metamorphosis from mature larva to adult with diet-reared larvae and adults exhibiting significantly higher lipid contents than foliage-reared insects. Regardless of larval food, newly eclosed adults tended to exhibit a decrease in the % of C18:3, and increases in C16:0 and C18:1 compared to larvae. Larval diet clearly influenced the fatty acid composition of larvae and adults, but only the % of C18:2 did not change between food, larvae and adults.