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J. Insecl Physiol. Vol. 34, No. 6, pp. 515-525, 1988 0022-1910/88 $3.00 + 0.00 Printed in Great Britain. All rights reserved Copyright 0 1988 Pergamon Press plc THE CAUSE OF REDUCED GROWTH OF MANDUCA SEXTA LARVAE ON A LOW-WATER DIET: INCREASED METABOLIC PROCESSING COSTS OR NUTRIENT LIMITATION? MICHAEL M. MARTIN and HEIDI M. VAN’T HOF Department of Biology, University of Michigan, Ann Arbor, MI 48109, U.S.A. (Received 28 July 1987; revised 9 November 1987) Abstract-Relative growth rates and nitrogen accumulation rates are lower for third-instar ~Uanduca sexta larvae on an artificial diet containing 65% water than on one containing 82% water, due to reduced efficiencies of conversion of digested food and digested nitrogen into larval biomass. Uric acid production is [email protected] greater, and non-feeding respiration rates 16.0% higher in the larvae on the low-water diet. Food is the major source of water for the larvae, with metabolic water making only a minor contribution to water input. Faecal excretion is the major avenue of water loss, although a significant amount of water is also lost by transpiration. Larvae from the low-water diet retain and use a higher percentage of the water they gain than larvae from the high-water diet (49.4% vs 41.9%). They produce much drier faeces (48.1% water vs 77.3% water), and, because their tissues are less hydrated (81.3% water vs 88.1% water), they synthesize 70% more new, fully hydrated tissue from a given amount of water than larvae from the high-water diet. We discuss problems involved in the use of determinations of efficiency of conversion of digested food in establishing causal links between diet, growth, and metabolic maintenance costs, and also offer a definition of food processing costs that distinguishes them from metabolic costs attributable to other processes, such as food acquisition, growth, and moulting. We conclude that reduced growth and reduced efficiency of conversion of digested food on low-water diets are due to limitation in the amount of water available for the synthesis of new hydrated tissue, and not to the imposition of higher food processing costs. Key Word Index: Tobacco hornworm, Manduca sex& growth, nutritional indices, food utilization, nitrogen budget, water budget, uric acid production, respiration rates, metabolic maintenance costs, food processing costs INTRODUCIION growth is carbon-limited, in which case any carbon allocated to energy metabolism is not available for The growth rates of herbivorous lepidopteran larvae the production of new tissue. However, when growth are strongly dependent upon the water content of is not carbon-limited, a high metabolic maintenance their food (Scriber, 1977; Reese and Beck, 1978; cost could be the consequence, rather than the cause, Scriber and Feeny, 1979; Timmins et al., 1987). of a low growth rate. For example, if water were Significantly reduced larval growth rates on diets low growth-limiting then other potentially useful nutri- in water are due primarily to reduced efficiencies of ents assimilated from the diet would be present in converting assimilated material into larval biomass amounts exceeding those that could be used for rather than to reduced consumption rates or reduced growth. They would then have to be excreted, and assimilation efficiencies. Since efficiency of conversion since excretory processes are endergonic the elimi- of digested food reflects the allocation of assimilated nation of these surplus nutrients would add to the food to growth vis a vis energy metabolism, the lower total expenditure of energy by the larva. The Laws values of this efficiency have been interpreted as an and Conservation of Energy and Mass require only indication of higher metabolic maintenance costs for that the growth rate and metabolic maintenance costs larvae on a low-water diet (Slansky and Scriber, of a larva ingesting a fixed amount of food covary 1985). Although this interpretation is a valid applica- inversely, but it is not possible a priori to specify tion of the Laws of Conservation of Energy and whether a change in growth rate is the cause or Conservation of Mass to the larval energy budget, a consequence of a change in metabolic rate. number of unwarranted interpretations of causal Deciding whether reduced growth on a low-water links between diet and growth, formulated within the diet is the cause or effect of increased expenditure of context of an analysis of the energy and mass budgets metabolic energy is not a trivial semantic issue. It is of larval growth, have begun to appear regularly in tantamount to identifying the adaptive mechanisms the literature of nutritional ecology. For example, it that permit a herbivorous insect to exploit dry foliage is often implied that a high metabolic maintenance as food. If a low-water diet imposes high metabolic cost, inferred from a low efficiency of conversion of costs, which in turn cause efficiency of conversion of digested food, must be the cause of a low growth rate. ingested food and growth rate to be low, then selec- The assumption underlying this interpretation is that tion should favour energy efficiency in those pro- 515 516 MICHAEL M. MARTIN and HEIDI M. VAN’T HOF cesses that are responsible for the high metabolic duca sexta larvae on artificial diets containing costs. On the other hand, if the upper limit to the different amounts of water. The results have allowed amount of new larval tissue that can be synthesized us to address the question of whether reduced growth is set by the amount of water acquired from the diet, on a low-water diet is due to increased processing then selection should favour adaptations that extract costs or to limitations in the amount of water avail- and conserve the maximal amount of water from the able for growth. Our conclusion is that although food, even if those adaptations are energetically there is a directly measurable increase in the cost of costly. processing the low-water diet, it is the absolute Another common, albeit less serious, misuse of amount of water available that is responsible for terminology that has begun to appear in discussions reduced growth. While our work was in progress an of the consequences of dietary specialization is the excellent series of papers on the food intake, con- designation of high metabolic maintenance costs, version efficiency, water economy, and feeding behav- inferred from a low efficiency of conversion of inges- ior of fifth-instar M. sextu larvae has appeared ted food, as high “processing costs” for a given food. (Reynolds et al.. 1985, 1986; Timmins et al., 1987). “Processing cost” is an inappropriate term, because an insect’s maintenance costs involve the expenditure MATERIALS AND METHODS of energy on many processes that are not directly related to the processing of food. If the term “pro- Insects cessing cost” is destined to become a part of the Tobacco hornworms, Manduca sexta, were reared jargon of nutritional ecology, it needs to be given a from eggs (Carolina Biological Supply) on an precise definition. We offer the following. A pro- artificial diet (Bio-Serv no. 9783) containing 82% cessing cost is a metabolic cost imposed by the water at 24°C under 16 h light-8 h dark. operation of physiological and biochemical processes involved in extracting useful nutrients from ingested Determination of growth, food consumption andfaecal food, eliminating waste products generated during production the processing of the food, and countering the poten- Third-instar larvae, collected within one-half hour tial harmful effects of toxins or other non-nutrient of moulting, were weighed and placed individually chemicals present in the food. Processing costs into IO-ml shell vials containing preweighed portions would, therefore, include the synthesis and secretion of artificial diet (Bioserv no. 9783) initially containing of digestive enzymes, the synthesis and secretion of either 82 or 65% water. The diet was held in place the peritrophic membrane. the physical alteration within the vial by a stainless steel pin inserted into the and movement of material within the gut, the main- aluminum foil-wrapped rubber stopper. In order to tenance of appropriate ion and water fluxes between maximize the accuracy of the nutritional indices the haemocoel and the gut, the maintenance of gut calculated from these measurements (Schmidt and pH, the assimilation and absorption of nutrients, the Reese, 1986) the quantity of food supplied was resorption of water from the hindgut, the trans- limited such that at least 75% was consumed by the formation of assimilated nutrients into a metabolite larvae during the instar. The vials containing the pool useful as a source of biosynthetic precursors or larvae and their food were placed in an incubator metabolic fuels, the synthesis and excretion of meta- (24°C 16 h light-8 h dark) until the larvae moulted to bolic waste products, and the activation and oper- the fourth instar. Toward the end of the instar the ation of detoxification processes. This definition ex- larvae were observed every half hour, so that the time cludes costs associated with foraging or feeding, of the moult, and hence the duration of the instar, which we propose should be classified as acquisition was known to within one-half hour. As soon as the costs. Acquisition costs may also depend to some larvae had moulted to the fourth instar, larvae, faeces extent upon the physical and chemical characteristics and uneaten food were separated and dried to con- of the diet, but they will be far more dependent upon stant weight in an oven at 75°C. The dry weights of microclimatic conditions, habitat structure, the prox- the larvae at the beginning of the experiment were imity of conspecifics, and other environmental fac- calculated from a live weight vs dry weight cali- tors.

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