Balancing of specific nutrients and subsequent growth and body composition in the slug Arion lusitanicus

Abstract

Feeding generalists typically occupy broad ecological niches and so are potentially pre-adapted to a range of novel food objects. In northern Europe, the slug Arion lusitanicus has spread rapidly as an invasive species and a serious horticultural and agricultural pest. We used nutritional geometry to analyze nutrient balancing capabilities and consequences for performance in A. lusitanicus when provided with one of three nutritionally fixed diets or when given dietary choice. The slugs over-ingested high amounts of the most abundant nutrient in order to get more of the limited nutrient. However, they regulated protein intake more tightly than carbohydrate intake resulting in a very high food intake when fed a protein-poor diet. Growth and body composition were highly affected by the nutrient balance of their diet. When given the choice to feed from two nutritionally different diets, the slugs selected an intake balance of protein and carbohydrate with sufficient precision to maximize growth. Nutrient utilization efficiency increased with increasing deficiency of the specific nutrient in the diet. Ingested carbohydrate was more efficiently stored as lipid in slugs fed more carbohydrate-poor diets, and ingested nitrogen was more efficiently incorporated into slug bodies in slugs fed more protein-poor diets. Our experiments suggest that the evolved behavioral and physiological regulatory capacities of A. lusitanicus may explain some of the success that this slug experiences as an invasive species. We furthermore propose that invasive species might be more dependent on high protein availability in the environment than non-invasive species.

Adaptive contraction of diet breadth affects sexual maturation and specific nutrient consumption in an extreme generalist omnivore

“…With the exception of GA females fed glucose‐containing diets, the rule of compromise used by the cockroaches in our experiment strongly supports the theory that omnivores eat until their protein requirements are covered but do not overingest large amounts of protein (Fig. ), known as the protein leverage hypothesis (Sørensen et al ., ; Jensen et al ., ). It is becoming increasingly clear that protein has a deleterious effect if present at a high ratio in the diet, with reduced lifespan as a consequence (Lee et al ., ; Maklakov et al ., ; Schmehl et al ., ; Solon‐Biet et al ., ).…”

“…Optimal foraging theory predicts that animals have evolved adaptations to forage optimally in their environment (Stephens & Krebs, ; Waldbauer & Friedman, ), and optimal foraging has more recently been extrapolated to the intake composition of specific nutrients (Simpson & Raubenheimer, ). Thus, a wide range of animals, including herbivores (Simpson et al ., ; Behmer, ), omnivores (Raubenheimer & Jones, ; Lee et al ., ; South et al ., ; Jensen et al ., ), and predators (Mayntz et al ., ; Jensen et al ., ), have been shown to forage selectively to balance the intake of multiple nutrients and thereby maximize fitness‐determining traits. Nutrient balancing might have to be compromised, however, if some foods in the environment are deterrent or toxic, forcing animals to forage for a balanced nutrient intake while avoiding ingestion of deleterious compounds to survive and perform optimally.…”

Effects of foraging distance on macronutrient balancing and performance in the German cockroach,Blattella germanica

“…Higher protein intake is known to increase growth rate in insects and other invertebrates (Behmer, 2009;Jensen et al, 2011Jensen et al, , 2013, and individuals with a higher growth rate can more rapidly escape predation from similarsized predators as they become too large to handle (Ludwig and Rowe, 1990;Price et al, 1980). At a higher growth rate, individuals are also more likely to reach the adult stage and reproduce before being killed by a predator.…”

“…The positive correlations between nutrient-specific consumption and performance outcomes further indicate that ingested nutrients were utilized at similar efficiency regardless of foraging distance. Different utilization of specific nutrients after ingestion has been shown in a number of invertebrates when restricted to nutritionally imbalanced diets over longer periods (Jensen et al, 2011(Jensen et al, , 2013Lee et al, 2002Lee et al, , 2003Simpson et al, 2002), and involves reduced utilization efficiency of the abundant nutrient to facilitate larger overall consumption and therefore larger ingestion of the deficient nutrient. At longer distances between individually imbalanced food sources than in the present experiment, different utilization of ingested nutrients would be likely to occur if individuals stay increasingly longer at located foods as the distance between foods increases, and they would therefore ingest more nutritionally imbalanced food before searching for a complementary food source Bernays et al, 1997).…”

“…While the consumption of one food alone does not satisfy all nutritional needs, selective consumption of an assortment of foods allows an individual to compose a balanced diet (Simpson and Raubenheimer, 1996;Simpson and Simpson, 1992;Thompson and Redak, 2000), and consequently maximize fitness-determining traits such as growth and reproduction (Jensen et al, 2012(Jensen et al, , 2013Lee et al, 2008;Raubenheimer and Jones, 2006;Simpson et al, 2004Simpson et al, , 2015. Indeed, a wide range of animals are shown to self-select a balanced diet when given dietary choice .…”