Social and nutritional factors shape larval aggregation, foraging, and body mass in a polyphagous fly

Abstract

The majority of insect species have a clearly defined larval stage during development. Larval nutrition is crucial for individuals’ growth and development, and larval foraging success often depends on both resource availability and competition for those resources. To date, however, little is known about how these factors interact to shape larval development and behaviour. Here we manipulated the density of larvae of the polyphagous fruit fly pest Bactrocera tryoni (‘Queensland fruit fly’), and the diet concentration of patches in a foraging arena to address this gap. Using advanced statistical methods of machine learning and linear regression models, we showed that high larval density results in overall high larval aggregation across all diets except in extreme diet dilutions. Larval aggregation was positively associated with larval body mass across all diet concentrations except in extreme diet dilutions where this relationship was reversed. Over time, larvae in low-density arenas also tended to aggregate while those in high-density arenas tended to disperse, an effect that was observed for all diet concentrations. Furthermore, larvae in high-density arenas displayed significant avoidance of low concentration diets – a behaviour that was not observed amongst larvae in low-density arenas. Thus, aggregation can help, rather than hinder, larval growth in high-density environments, and larvae may be better able to explore available nutrition when at high-density than when at low-density.

Interactions between ecological factors in the developmental environment modulate pupal and adult traits in a polyphagous fly

“…Previous studies in other species corroborate these effects of sugar-rich diets in larval development (see for instance Matavelli et al, 2015;Silva-Soares, Nogueira-Alves, Beldade, & Mirth, 2017;Zucoloto, 1987Zucoloto, ,1991. Spatial aggregation is known to occur across insect species (Taylor, 1961), including B. tryoni (Morimoto et al, 2018); larval movement between fruits remains subject of further investigation. Given that the nutritional composition of fruits varies across strata within fruits (spatial variation) as well as during the ripening process (temporal variation) (Janzen, 1977;Matavelli et al, 2015), larvae could migrate to and aggregate in different strata within a fruit and potentially (although less likely) move from one fruit to another in more nutritious ripening conditions.…”

“…Given that the nutritional composition of fruits varies across strata within fruits (spatial variation) as well as during the ripening process (temporal variation) (Janzen, 1977;Matavelli et al, 2015), larvae could migrate to and aggregate in different strata within a fruit and potentially (although less likely) move from one fruit to another in more nutritious ripening conditions. Spatial aggregation is known to occur across insect species (Taylor, 1961), including B. tryoni (Morimoto et al, 2018); larval movement between fruits remains subject of further investigation.…”

“…Nutrient-poor larval diets created by high larval densities have been shown to delay pupation, increase pupal mortality, and result in small adult body size (Gage, 1995;Morimoto, Pizzari, & Wigby, 2016;Stockley & Seal, 2001). If larvae are foraging in nutrient-poor diets, the costs of nutrient limitation and competition in larval aggregations can be high and rapidly offset the benefits of aggregation, and thus, larval aggregation patterns tend to be diet-dependent (Morimoto et al, 2018). If larvae are foraging in nutrient-poor diets, the costs of nutrient limitation and competition in larval aggregations can be high and rapidly offset the benefits of aggregation, and thus, larval aggregation patterns tend to be diet-dependent (Morimoto et al, 2018).…”

“…Larvae of many insects tend to aggregate in high density (Durisko & Dukas, 2013;Ives, 1991;Taylor, 1961;Taylor, Woiwod, & Perry, 1978) often with positive effects on individual fitness across taxa, including Diptera, Coleoptera, and Lepidoptera (the "Allee effect" [Allee, Park, Emerson, Park, & Schmidt, 1949;Courchamp, Clutton-Brock, & Grenfell, 1999]; see e.g., Appleby & Credland, 2007;Lawrence, 1990;Morimoto, Nguyen, Tarahi Tabrizi, Ponton, & Taylor, 2018;Weaver & Mcfarlane, 1990). Despite this, the positive effects of aggregation depend on diet composition.…”

“…This is likely because high larval density decreases the availability of protein (and consequently amino acids) to the developing larvae (Klepsatel, Procházka, & Gáliková, 2018). If larvae are foraging in nutrient-poor diets, the costs of nutrient limitation and competition in larval aggregations can be high and rapidly offset the benefits of aggregation, and thus, larval aggregation patterns tend to be diet-dependent (Morimoto et al, 2018). However, diet quality is defined not only by its nutritional composition but also by its microbial community.…”