Measuring Caenorhabditis elegans Spatial Foraging and Food Intake Using Bioluminescent Bacteria

Abstract

For most animals, feeding includes two behaviors: foraging to find a food patch and food intake once a patch is found. The nematode Caenorhabditis elegans is a useful model for studying the genetics of both behaviors. However, most methods of measuring feeding in worms quantify either foraging behavior or food intake, but not both. Imaging the depletion of fluorescently labeled bacteria provides information on both the distribution and amount of consumption, but even after patch exhaustion a prominent background signal remains, which complicates quantification. Here, we used a bioluminescent Escherichia coli strain to quantify C. elegans feeding. With light emission tightly coupled to active metabolism, only living bacteria are capable of bioluminescence, so the signal is lost upon ingestion. We quantified the loss of bioluminescence using N2 reference worms and eat-2 mutants, and found a nearly 100-fold increase in signal-to-background ratio and lower background compared to loss of fluorescence. We also quantified feeding using aggregating npr-1 mutant worms. We found that groups of npr-1 mutants first clear bacteria from within the cluster before foraging collectively for more food; similarly, during large population swarming, only worms at the migrating front are in contact with bacteria. These results demonstrate the usefulness of bioluminescent bacteria for quantifying feeding and generating insights into the spatial pattern of food consumption.

Comparison of solitary and collective foraging strategies of Caenorhabditis elegans in patchy food distributions

“…Both strains crawl at about the same speed in the absence of food; N2 worms slow down to roughly half this speed when on food, whereas npr-1 worms only slow down significantly upon joining a group of worms on food (16). Secondly, npr-1 worms have a feeding rate that is 62% that of N2, as calculated by us previously (28). These literature parameters are listed in Table 1 and adapted for our strain-specific simulations; model parameters are listed in Table 2.…”

“…In this strain-specific model, agents perceive food only from the lattice sites that they currently occupy. * Feeding rates in the strain-specific model are scaled down to 0.4 for N2 and 62% of that for npr-1 (28) to broadly match the experimental time to food depletion in Figure 5, based on a time step of Δt = 10 s.…”

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

“…Feeding rates in the strain-specific model are scaled down to 0.4 for N2 and 62% of that for npr-1(28) to broadly match the experimental time to food depletion inFigure 5, based on a time step of Δt = 10 s.…”

Inversion of pheromone preference optimizes foraging in C. elegans

“…This first factor has been thoroughly studied both theoretically and experimentally in the context of optimal foraging and the marginal value theorem ( Charnov, 1976 ; Krebs et al, 1978 ; Oaten, 1977 ; Stephens and Krebs, 1987 ; Watanabe et al, 2014 ), and in this respect, our model simply reproduces previous results. A recent paper on C. elegans foraging contradicts this general assumption of diminishing returns, showing a near-linear depletion of food patches ( Ding et al, 2020 ). This result was obtained in laboratory conditions, with very rich and uniform food patches, which may not reflect natural ones, but at least indicates that the general assumption of diminishing returns is relatively easy to break, and opens the question of whether more care should be put in assessing the conditions in which current optimal foraging models are applicable.…”