Underlying mechanisms and ecological context of variation in exploratory behavior of the Argentine ant, Linepithema humile

Abstract

Uncovering how and why animals explore their environment is fundamental for understanding population dynamics, the spread of invasive species, species interactions, etc. In social animals, individuals within a group can vary in their exploratory behavior, and the behavioral composition of the group can determine its collective success. Workers of the invasive Argentine ant (Linepithema humile) exhibit individual variation in exploratory behavior, which affects the colony's collective nest selection behavior. Here, we examine the mechanisms underlying this behavioral variation in exploratory behavior and determine its implications for the ecology of this species. We first establish that individual variation in exploratory behavior is repeatable and consistent across situations. We then show a relationship between exploratory behavior and the expression of genes that have been previously linked with other behaviors in social insects. Specifically, we found a negative relationship between exploratory behavior and the expression of the foraging (Lhfor) gene. Finally, we determine how colonies allocate exploratory individuals in natural conditions. We found that ants from inside the nest are the least exploratory individuals, whereas workers on newly formed foraging trails are the most exploratory individuals. Furthermore, we found temporal differences throughout the year: in early-mid spring, when new resources emerge, workers are more exploratory than at the end of winter, potentially allowing the colony to find and exploit new resources. These findings reveal the importance of individual variation in behavior for the ecology of social animals.

Keywords: Behavioral ecology; Collective behavior; Exploration; Foraging; Gene expression; Invasive species; Personality; Repeatability.

Fig. 1.

Quantifying exploration. (A) The eight-armed maze used for quantifying exploration. (B,C) Walking trajectories (green lines) of Argentine ants (Linephithema humile) walking in an open field for 5 min. These ants made 0 (B) and 5 (C) visits to spices when tested in the eight-armed maze the previous day.

Fig. 2.

Quantifying trail use. Trail density, measured as number of ants crossing an invisible line on the trail during 30 s. Values are averages of three counts on each high- and low-use trail, at the end of winter (A) and in early-mid spring (B) in four colonies. Points are averages of three counts and error bars are the standard deviation of these counts. Each colony is denoted by a different shape. Points and error bars are slightly jittered along the x-axis to improve visibility.

Fig. 3.

Exploratory behavior across settings. A significant positive correlation between the exploratory behavior of an ant when measured in the eight-armed maze and the travel path length in an open field. Points are slightly jittered along the x-axis to improve visibility.

Fig. 4.

Exploratory behavior related to gene expression. A significant negative correlation between exploratory behavior (number of visits to spices in the eight-armed maze) and the expression of the Lhfor gene (relative gene expression normalized to GAPDH). Error bars are standard errors. Points are slightly jittered along the x-axis to improve visibility.

Fig. 5.

Exploratory behavior in nature. Exploratory behavior of L. humile workers collected from different locations: low- and high-use foraging trails, and from inside the nest in the (A) late winter and (B) early-mid spring. Boxes indicate the lower and upper quartiles; horizontal lines within boxes indicate the median; whiskers extend to the 1.5 interquartile range from the box; and open circles indicate outliers. Boxes that do not share a letter are statistically different according to a post hoc Tukey test (P<0.01).