Comparison of solitary and collective foraging strategies ofCaenorhabditis elegansin patchy food distributions

Abstract

Collective foraging has been shown to benefit organisms in environments where food is patchily distributed, but whether this is true in the case where organisms do not rely on longrange communications to coordinate their collective behaviour has been understudied. To address this question, we use the tractable laboratory model organism Caenorhabditis elegans, where a social strain (npr-1 mutant) and a solitary strain (N2) are available for direct comparison of foraging strategies. We first developed an on-lattice minimal model for comparing collective and solitary foraging strategies, finding that social agents benefit from feeding faster and more efficiently simply due to group formation. Our laboratory foraging experiments with npr-1 and N2 worm populations, however, show an advantage for solitary N2 in all food distribution environments that we tested. We incorporated additional strainspecific behavioural parameters of npr-1 and N2 worms into our model and computationally identified N2's higher feeding rate to be the key factor underlying its advantage, without which it is possible to recapitulate the advantage of collective foraging in patchy environments. Our work highlights the theoretical advantage of collective foraging due to group formation alone without long-range interactions, and the valuable role of modelling to guide experiments.

MeasuringC. elegansspatial foraging and food intake using bioluminescent bacteria

“…While N2 worms show gradual depletion of the whole food patch roughly uniformly (Figure 3C, top row; Supplementary Movie S1, middle row), DA609 worms deplete food in a highly localised manner starting at one point and sweeping over the surface (Figure 3C, bottom row; Supplementary Movie S1, top row). These foraging behaviours observed here by bacterial depletion are consistent with our previous results in which worms were imaged directly (Ding, Schumacher, et al 2019).…”

“…Moreover, we noticed that when DA609 worms initially aggregate they are covered in bacteria (Figure 3C-D, 30 min panels) and that the cluster stays in roughly the same place (Figure 3C-D, red circles) until the in-cluster bacteria are completely consumed. This observation fits well with the distinct “aggregation” versus “swarming” phases that we previously reported for DA609 ( npr-1 ) aggregation (Ding, Schumacher, et al 2019), suggesting that minimal cluster movement during the “aggregation” phase is due to the initial food availability inside the cluster. By contrast, the total depletion of bacteria inside the aggregate before collective movement starts is difficult to detect from the recordings of worms feeding on fluorescent bacteria, because the moving worm cluster is still fluorescent (Figure 1A, last panel; note the aggregation timescale is different for this experiment because OP50-DsRed bacteria were diluted).…”

“…However, when we recorded worms feeding on E. coli strain OP50-DsRed, we noticed a prominent background fluorescence signal, which was especially conspicuous in our experiments with DA609 ( npr-1 aggregation mutant) worms (Figure 1A, red arrow). These worms first form aggregates on food and then collectively swarm over the food patch following local food depletion (Ding, Schumacher, et al 2019). It is possible that a fraction of DsRed molecules survives passage through the worm gut due to resistance to protease cleavage.…”

“…To gain insights into different C. elegans feeding strategies, we performed experiments with the laboratory reference strain N2 and DA609, an npr-1 loss-of-function mutant. The former are solitary feeders whereas the latter are social, initially forming worm aggregates on food and then collectively swarming over the food patch following local food depletion (Ding, Schumacher, et al 2019). Our feeding experiments on DH5α-ilux bioluminescent bacteria show that DA609 and N2 populations both have stable feeding rates, and that DA609 has a feeding rate that is 58% that of N2 (Figure 3A-B).…”

“…How food is distributed and consumed in space has crucial implications for animal foraging strategy (Bernstein 1975; Ding, Muhle, et al 2019; Lanan 2014; Stenberg and Persson 2005) and subsequent fitness. Therefore, of the existing methods of quantifying feeding, imaging the consumption of fluorescently-labelled bacteria is of particular interest since it can provide information on both where and how much food has been consumed.…”