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

Abstract

18The majority of insect species have a clearly defined larval stage during development. Larval 19 nutrition is crucial for individuals' growth and development, and larval foraging success 20 often depends on both resource availability and competition for those resources. To date, 21 however, little is known about how these factors interact to shape larval development and 22 behaviour. Here we manipulated the density of larvae of the polyphagous fruit fly pest 23Bactrocera tryoni ('Queensland fruit fly'), and the diet concentration of patches in a foraging 24 arena to address this gap. Using advanced statistical methods of machine learning and linear 25 regression models, we showed that high larval density results in increased larval aggregation 26 across all diets except in extreme diet dilutions. Larval aggregation was positively associated 27 with larval body mass across all diet concentrations except in extreme diet dilutions where 28 this relationship was reversed. Larvae in low-density arenas also tended to aggregate while 29 those in high-density arenas tended to disperse, an effect that was observed for all diet 30concentrations. Furthermore, larvae in high-density arenas displayed significant avoidance of 31 low concentration dietsa behaviour that was not observed amongst larvae in low-density 32 arenas. Thus, aggregation can help, rather than hinder, larval growth in high-density 33 environments, and larvae may be better able to explore available nutrition when at high-34 density than when at low density. 35 36 37 38 110 Predictions 1111) Previous studies in other species have shown that larvae prefer to occupy patches that 112 are shared with conspecifics [e.g., 45 ]. Thus, we predicted that an increase in larval 113 density should increase aggregation formation as well as aggregation size amongst 114 diet patches. However, this effect could be diet-dependent, whereby macronutrient-115 poor diets could support smaller aggregations whereas macronutrient-rich diets would 116 support larger aggregations. As a result, we predicted that aggregates should be 117 smaller in macronutrient-poor diets than in macronutrient-rich diets; 1182) In other insects, larval aggregation can facilitate feeding [e.g., 40 ]. We therefore 119 predicted that treatments with high larval aggregations should have larvae with higher 120 body mass. However, macronutrient-poor diet is known to reduce larval body mass 121 (see 'Introduction'). As a result, we predicted that larval body mass should be lower 122 in macronutrient-poor diets compared with macronutrient-rich diets; 123 124 Materials and Methods 125 Fly stock and egg collection 126We collected eggs from a laboratory-adapted stock of B. tryoni (>17 generations-old). The 127 colony has been maintained in non-overlapping generations in a controlled environment room 128(humidity 65 ± 5%, temperature 25 ± 0.5 o C) with light cycle of 12h light: 0.5h dusk:11h 129 dark: 0.5h dawn). Adults were provided a free-choice diet of hydrolysed yeast (MP 130 Biomedicals, Cat. n o 0210330...

Nutritional availability and larval density dependence in Aedes aegypti

“…Larval aggregation commonly occurs in many insect species (Taylor, 1961) and can confer behavioural and physiological benefits that promote larval development, provided that the benefits of aggregation are not outweighed by the costs of competition (Cornell et al, 1987;Durisko & Dukas, 2013). For example, Morimoto et al (2018) observed complex interactions between larval density, foraging behaviour, and development in polyphagous fruit flies (Bactrocera tryoni), observing that larval aggregation resulted in consistently higher body mass but that very high larval densities resulted in increased dispersion of larvae (Morimoto et al, 2018). It is possible that higher densities of Ae.…”

Integrative developmental ecology: a review of density-dependent effects on life-history traits and host-microbe interactions in non-social holometabolous insects

“…The literature of density-dependent effects in holometabolous insects is a fruitful ground for terms referring to population density, including (but not limited to) 'low and high density' [e.g., (Henry et al 2020; Ower and Juliano 2019)], 'aggregation' (Inouye and Johnson 2005;Morimoto et al 2018), 'crowding' [e.g. (Lushchak et al 2019Morimoto et al 2019a)] and 'overcrowding' (Ikeshoji and Mullai 1970;Roberts 1998) (the authors are themselves guilty of contributing to such panacea of terms).…”

“…Despite the general trends described above, some fly species benefit from high density via faster developmental pace. For instance, high larval density in some blowfly and fruit fly species can lead to benefits of group feeding that shortens developmental time [e.g., Calliphora vicina (Saunders and Bee 2013); Phormia regina (Green et al 2002); B. tryoni (Morimoto et al 2018). In blowflies in particular, shorter developmental time in high larval densities is likely an evolutionary response to the nutritional ecology of Calliphoridae species which feed on carcass, an ephemeral resource attractive to many species.…”

Density-by-diet interactions during larval development shape adult life-history trait expression and fitness in a polyphagous fly

“…Eggs are deposited in small batches of 4-20 eggs per oviposition bout, and several females lay eggs in the same fruit so that offspring densities can vary (Fitt 1986, 1990). In addition, larvae are known to aggregate in a diet-dependent fashion with potential fitness benefits but also with costs of increasing intraspecific competition (Christenson and Foote 1960; Morimoto et al 2018). Based on ecological theory and previous studies of density- and diet-dependent effects, we obtained the predictions highlighted in Table 1.…”

“…Herbivorous holometabolous insects are ideal to study individual-and population-level effects of developmental ecological factors. This is because ecological factors that influence the quality of larval developmental environment in herbivorous insects are relatively simple to model [e.g., (Atkinson and Shorrocks 1981)] and manipulate [e.g., (Morimoto et al 2018)], and display longlasting quantifiable effects on fitness [e.g., (Rossiter 1992;Steigenga and Fischer 2009;Takken et al 2013;Tigreros 2013;Matavelli et al 2015;Rodrigues et al 2015;Morimoto et al 2016Morimoto et al , 2019bSchwab et al 2017;Than et al 2020)]. This is ideal for controlled experimental approaches that envisage to test theories and provide new empirical evidence to guide further ecological research assessing the quality of developmental environments, particularly because the concept and scope of (developmental) habitat can be complex to define and properly measure in uncontrolled environments (Mitchell 2005).…”