Collective foraging decision in a gregarious insect
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- Lihoreau, M., Deneubourg, J. & Rivault, C. Behav Ecol Sociobiol (2010) 64: 1577. doi:10.1007/s00265-010-0971-7
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Group foraging by eusocial insects implies sophisticated recruitment processes that often result in collective decisions to exploit the most profitable sources. These advanced levels of cooperation, however, remain limited to a small range of species, and we still know little about the mechanisms underlying group foraging behaviours in the great mass of animals exhibiting lower levels of social complexity. In this paper, we report, for the first time in a gregarious insect, the cockroach Blattella germanica (L.), a collective foraging decision whereby the selection of food sources is reached without requiring active recruitment. Groups of cockroaches given a binary choice between identical food sources exhibited exploitation asymmetries whose amplitude increases with group size. By coupling behavioural observations to computer simulations, we demonstrate that selection of food sources relies uniquely on a retention effect of feeding individuals on newcomers without comparison between available opportunities. This self-organised pattern presents similarities with the foraging dynamics of eusocial species, thus stressing the generic dimension of collective decision-making mechanisms based on social amplification rules despite fundamental differences in recruitment processes. We hypothesise that such parsimony could apply to a wide range of species and help understand the emergence of collective behaviours in simple social systems.
KeywordsCollective decision makingForaging behaviourGregarious cockroachesRetention effect
Organisms routinely have to make decisions that are crucial for their fitness, whether this be choosing food locations, breeding sites or mating partners. When facing key decisions, we humans rarely act completely by ourselves, but usually rely on the advice of others to optimise choices (Salganik et al. 2006; Dyer et al. 2008). Like us, many animals improve their personal knowledge by gleaning social information from other members of their group (Danchin et al. 2004; Dall et al. 2005; Leadbeater and Chittka 2007) so that individuals in a group make faster and more accurate decisions than their lone conspecifics (Valone and Templeton 2002; Simons 2004).
Foraging decision making by group-living animals has traditionally been approached by game theoretic models based on economic interdependence between individual payoffs (Fretwell 1972; Giraldeau and Caraco 2000). Whilst this well-developed modelling platform focuses on the adaptive significance of individual decisions, foraging outcomes are, however, also expected to depend on underlying decision-making mechanisms whose properties cannot be understood as the simple addition of individual contributions. In recent years, increasing interest in ‘collective decisions’ has provided new insights for investigating these decision-making processes, and this has become one of the hottest topics in behavioural biology (Parrish and Edelstein-Keshet 1999; Beekman et al. 2001; Marée and Hogeweg 2001; Couzin et al. 2005; Pratt and Sumpter 2006). Collective decisions generally refer to the behaviours of groups composed of solitary decision makers able to select jointly a single option out of many other alternatives through amplification processes, leading to symmetry breaking (Deneubourg and Goss 1989; Camazine et al. 2001; Couzin and Krauze 2003; Sumpter et al. 2008; Sumpter and Pratt 2009; Sumpter 2009). Such collective dynamics can lead to a more or less greater majority selecting an option, depending on whether it results from a ‘consensus’ among group members or a ‘combined decision’ that usually affects the largest part of the group (Conradt and Roper 2005). Just as an individual’s choice emerges from complex interactions of a network of neurons, a collective decision thus emerges from an analogous network of interacting individuals (Krause et al 2007; Hölldobler and Wilson 2008; Passino et al. 2008; Marshall and Franks 2009).
To date, the most important advances concerning collective foraging decisions come no doubt from the study of eusocial insects (i.e. ants, bees, wasps and termites) that exhibit task specialisation and altruistic behaviours related to kin selection (Camazine and Sneyd 1991; Beckers et al. 1992; Nicolis and Deneubourg 1999; Sumpter and Pratt 2003). In these species, workers that discover profitable food sources convey attraction signals to their nestmates and trigger the onset of a recruitment process. The foraging behaviour of recruited individuals is then influenced by positive feedbacks enhanced by chemical or tactile signals (e.g. pheromone trail deposit, waggle dance), leading progressively to selection and collective exploitation of the most profitable food sources by the colony (Hölldobler and Wilson 1990; Seeley 1995). Sophisticated recruitment processes (i.e. ‘active’ recruitment based on signalling) involved in these self-organised behaviours are nevertheless highly specific to eusociality that occurs only in a limited fraction of the wide spectrum of animal societies (Krause and Ruxton 2002; Costa 2006). Studies investigating collective decisions by non-eusocial species are less abundant (Jeanson et al. 2004; Amé et al. 2006; Buhl et al. 2006; Gautrais et al. 2007; Ward et al. 2008), but have the fundamental advantage of providing generic rules that can apply to a wider range of species and to different selection levels without invoking complex communication or interactions. Although individuals of many non-eusocial vertebrates [e.g. sheep (Sibbald and Hooper 2004) and tadpoles (Sontag et al. 2006)] and invertebrates [e.g. bark beetles (Grégoire 1988), caterpillars (Fitzgerald 1995), ladybirds (Hemptinne et al. 2000) and treehoppers (Cocroft 2005)] are known to aggregate and to exploit food patches collectively, their underlying decision-making mechanisms are still poorly understood. A few studies nevertheless suggest that despite the absence of complex recruitment processes, group decisions in these species could rely on non-linear dynamics based on social amplification rules similar to those described in eusocial species (Deneubourg et al. 1990; Dussutour et al. 2007). From our point of view, investigating collective decision-making mechanisms and their functional consequences in non-eusocial species constitutes a promising approach to reach a better understanding of the emergence of collective patterns and cooperative behaviours in simple social systems.
In this paper, we report a collective foraging decision in the gregarious cockroach Blattella germanica (L.). Our study provides completely new insights into the social biology of these cockroaches, up to now considered as solitary foragers (Durier and Rivault 2000a, b, 2001), and describes, for the first time to our knowledge, a foraging decision-making mechanism based uniquely on a retention effect without requiring active recruitment. We investigated both the mechanisms and the functions of the collective foraging decision by coupling behavioural observations and computer simulations. First, we analysed the foraging dynamics of groups of different sizes that were given a binary choice between two identical food sources. Second, we compared the foraging performances of isolated individuals to that of focal individuals in a group. Third, we built a decision-making model based on our observations and confronted computer simulation outputs to our experimental data.
Materials and methods
Study species and experimental setup
Group foraging dynamics
We investigated group foraging dynamics by testing cockroaches in the presence of two identical food sources (Fig. 1a). Experiments were performed with first-instar nymphs starved from hatching until being tested (4 days old) so that they had no feeding experience and were strictly all in the same physiological state. We tested groups of 50 (N = 27 replicates), 100 (N = 25 replicates) and 200 cockroaches (N = 19 replicates), thus covering ecologically realistic size and density ranges of aggregates in natural populations (Rivault 1989; Rust et al. 1995). We recorded, with scan sampling, the numbers of individuals in the shelter, exploring the arena and on each food source, at 1-min intervals. The food source that attracted the greater number of cockroaches during a test was defined as the winner source, and the source that attracted the lower number of cockroaches was defined as the loser source. Exploitation of both sources was considered asymmetrical if the numbers of cockroaches on each source, when the total number of feeding cockroaches peaked, differed significantly from a random distribution (binomial test: p < 0.05).
Individual foraging performances
We evaluated the benefits gained by an individual foraging collectively by comparing foraging performances of focal cockroaches in a group of 50 individuals (N = 78 replicates) to those of isolated cockroaches (N = 74 replicates) in the presence of a single food source (Fig. 1b). We recorded, by continuous observation, latency to leave the shelter, latency to reach the food source and the number and duration of each feeding bout at the source. Test cockroaches were marked individually with a drop of paint on their pronotum. Experiments were performed with starved sixth (last)-instar nymphs (45 days old) as they are more convenient to mark than first-instar nymphs. Preliminary experiments allowed us to validate our marking technique because comparison of foraging performances between marked and unmarked cockroaches did not reveal any significant differences in foraging behaviours (Wilcoxon test: marked N = 74; unmarked N = 40; latency to visit food: marked = 342. 67 ± 42.78 s, unmarked = 373.28 ± 36.37 s, W = 1,448.5, p = 0.854; number of feeding bouts: marked = 5.18 ± 0.56, unmarked = 5.93 ± 0.75, W = 1,566.5, p = 0.6059; feeding bout duration: marked = 211.18 ± 20.41 s, unmarked = 188.24 ± 22.74 s, W = 1,593, p = 0.5021; total feeding duration: marked = 896.58 ± 110.52 s, unmarked = 875.77 ± 128.77 s, W = 1,694.5, p = 0.2037).
Collective decision-making mechanism
We investigated the collective decision-making mechanism using computer simulations of a mathematical model based on our experimental observations (see details in “Results”). Parameters of the model were estimated from data recorded on cockroaches tested individually (N = 56 replicates) in the arena in the presence of two identical food sources (Fig. 1a). Test individuals were first-instar nymphs starved from hatching until being tested (4 days old). We recorded, with continuous observations, latencies to leave the shelter, to reach each of the two food sources and the number and duration of feeding bouts on each source (ESM Table 1).
Programming and data analysis
Data were analysed using R 2.2.1. (R Development Core Team 2007). The model was implemented in MATLAB 7.1 (The MathWorks, Natick, Massachusetts). We performed Wilcoxon tests to compare foraging performances of isolated and grouped individuals (i.e. time latencies to visit food sources, number of feeding bouts, duration of each feeding bout, total feeding durations). We used binomial tests to estimate the occurrence of asymmetrical exploitations of food sources (i.e. winner/loser) and the randomness of source choice (i.e. left/right) by groups. We used chi-square goodness-of-fit tests to compare frequencies of significant asymmetries between groups of different sizes and between experimental and theoretical data. Chi-square goodness-of-fit tests also allowed us to test the exponentiality of observed data. Means are given with standard errors.
Group foraging dynamics
Individual foraging performance
Collective decision-making mechanism
To incorporate automatically the random aspect of the process defined in the equation system (Eqs. 1a–1f), we used stochastic simulations of the numerical model. The different steps can be summarised as follows: (1) initial conditions: All individuals are in the shelter and (2) decision process: At each time step (second), the state of each individual was checked. The decision of each individual to adopt a new state depends on the comparison between the probability to change step and a random number sampled from a uniform distribution between 0 and 1. If this value is less than, or equal to, that probability, the individual adopts a new state. Distributions of the numbers of individuals in the different states were calculated in relation to time. Like in the experiments, exploitation of sources was considered asymmetrical if the numbers of individuals on each source, when the total number of feeding individuals peaked, differed significantly from a random distribution (binomial test: p < 0.05).
Values dj, K, η and T were estimated by fitting Eq. 2 to experimental data (text ESM 1, ESM Table 1). dj + K is equal to the probability of individually tested cockroaches to leave source i at visit j. Under the hypothesis of a retention effect, the probability δij(Xi) to leave a source decreases when the number of individuals feeding on the source increases. α, β1 and β2 remain constant.
A systematic analysis of the model revealed that the introduction of a single retention effect is sufficient to generate theoretical exploitation dynamics of food sources with similar amplitudes and time windows to those observed in our experiments for the three group sizes (Fig. 5b). The best fitting data for δij(Xi) were obtained with d1 = 0.0013, d2 = 0.002, K = 0.0035 and η = 2, T = 22, which are parameter values in agreement with our experimental measures on individually foraging cockroaches (text ESM 1, ESM Table 1). The model thus predicts an increase of proportions of significant asymmetries on sources in relation to group size from 3% in groups of 50 (chi-square test: χ2 = 0.09, df = 1, p = 0.7574) to 9% in groups of 100 (chi-square test: df = 1, χ2 = 2.18, p = 0.1399) and 35% in groups of 200 (chi-square test: df = 1, χ2 = 0.27, p = 0.6047), which is in accordance with our observations. The high level of congruence between experimental and theoretical data clearly shows that selection of a food source by a group results from short-range interactions between individuals that consist in a retention effect of feeding cockroaches on newcomers.
In this study, we present evidence of a collective foraging decision by a gregarious insect. We analysed in detail the complete decision-making process and revealed, for the first time to our knowledge, a simple mechanism whereby the selection of food sources is reached through a single retention effect without requiring active recruitment. The self-organised foraging behaviour we describe highlights important similarities with the well-documented foraging dynamics of eusocial insects (Seeley 1995; Hölldobler and Wilson 1990) and evidence the generic dimension of collective decision-making mechanisms based on social amplification rules despite fundamental differences in the sophistication levels of social interactions.
The combined analysis of our experimental and theoretical data sheds completely new insights into the social biology of B. germanica and of gregarious cockroaches in general. Whilst these cockroaches are known to remain in large, stable and cohesive aggregates during their resting phase, they were until now considered to be solitary foragers, implying selfish food search based on learning the positions and quality of resources in their home range (Durier and Rivault 2000a, b, 2001). Our study reveals that foraging cockroaches use social information to select food sources, leading to a collective exploitation of a single source out of other alternatives. Undoubtedly, information transfer occurs between feeding individuals and explorers. Our experimentally validated model clearly demonstrates that cockroaches are not attracted by feeding conspecifics over a long range, but rather retained after a close contact. This suggests that feeding cockroaches recruit ‘passively’ via chemical or tactile cues directly at the food source without the necessity of active signalling through pheromonal emission or recruitment behaviour. Short-range communication reduces the probability that an individual will leave a food source, thus triggering a positive feedback that amplifies the recruitment process and leads to the formation of temporary aggregates on the selected source. This self-organised dynamic is density-dependant so that the amplitude of exploitation asymmetries reaches a maximum in large groups. Our data suggest that a minimum group size (i.e. quorum) has to be reached for the collective decision to occur (Conradt and Roper 2005; Sumpter and Pratt 2009), implying that solitary foraging is certainly the main strategy at low population densities, as evidenced by previous studies in this species (Durier and Rivault 2000a, b, 2001).
Cockroaches not only select food sources collectively but also benefit from a social facilitation for feeding by increasing their individual foraging performance, thus highlighting the adaptive value of group foraging. Longer stays at food sources were not side effects of overcrowding as size of sources strictly precluded competition in our experiments. Although the social facilitation was evidenced for sixth-instar nymphs only, the fact that this social effect explains well the group dynamics of first-instar nymphs strongly suggests that it does occur at all developmental stages. Our result reinforce the idea that group-living allow cockroaches to increase their individual fitness and strengthen previous reports evidencing the role of social dependence in maintaining group cohesion in this species (Lihoreau and Rivault 2008; Lihoreau et al. 2009). Contrary to species organised in family units, like in many eusocial insects, the basic form of cooperation we report here occurs between unrelated individuals within mixed family groups of cockroaches and consequently may not directly rely on benefits of kin selection. We suspect that in addition to prolonged feeding durations, the presence of conspecifics can provide an accurate estimate of resource quality (e.g. Boulinier and Danchin 1997) and constitute a local cue favouring aggregation around the most profitable food sources. Group foraging could also be a strategy to decrease individual predation risk through dilution effect or to reduce physical stresses such as temperature or humidity loss (Dambach and Goehlen 1999). All these types of benefits are density-dependant so that individual fitness increases when the population is asymmetrically distributed between food sources (Moody et al 1996; Amé et al 2006; Sumpter 2009). Although more investigations are needed to clarify these points, our study stresses the role of ‘ecological’ benefits of group-living (in opposition to ‘genetic’ benefits) as potential factors for the evolution of collective behaviours and the emergence of cooperation in gregarious species (Costa 2006; Korb and Heinze 2008).
Interestingly, collective decisions by gregarious cockroaches emerge both when selecting food sources, as reported here, and when selecting shelters for resting (Amé et al. 2004, 2006; Jeanson et al. 2005; Jeanson and Deneubourg 2007a, b). Similar retention effects exerted by conspecifics already present on a resource are able to trigger group formation in both contexts without the requirement of sophisticated active recruitments. Experimentally validated models developed to describe these two collective decisions reveal that animals are able to assess the quality of resources and to exploit selected sources optimally without global information or explicit comparisons of available opportunities. All individuals explore their environment randomly and select a resource in relation to the number of conspecifics already on it. The mathematical approach we used has a well-established tradition of deconstructing seemingly complex decision-making events and explaining them in terms of simple snowball processes in other systems than gregarious cockroaches. The use of agent-based models to describe collective decision-making processes was initially developed to investigate the foraging behaviour of eusocial species and provides a powerful tool to study the emergence of collective patterns based on sophisticated communication systems (Camazine and Sneyd 1991; Beckers et al. 1992; Nicolis and Deneubourg 1999; Sumpter and Pratt 2003). Whilst these models classically approximate collective decisions by their stationary states, our study demonstrates that a similar modelling approach can be relevant to investigate transient phenomena, thus providing new opportunities to describe the entire dynamics of the processes from the emergence to the extinction of the collective behaviour. More importantly, the fact that models based on similar structures and relying on similar amplification rules can be developed to investigate collective decisions in eusocial as well as in gregarious species despite important differences in recruitment processes highlights the generic aspect of self-organised decision-making mechanisms in group-living animals. The elegance of these parsimonious foraging systems is that the collective decision arises from the perception of conspecifics without the need for a leader having a synoptic overall view of the situation and knowing all the available options.
We predict that the minimal mechanism we describe, modulated by quantitative changes due to specific traits, should prove relevant to explore collective foraging strategies in a wide array of group-living species with varying levels of social complexity. Similar retention effects should also be involved in a wider range of contexts, as it has been shown for aggregation dynamics in cockroaches and recently suggested for nest selection by ants (Robinson et al. 2009). Investigating the power and limits of these decision-making processes to describe group dynamics in very different systems should greatly help further our understanding of the emergence collective behaviours and cooperation in their simplest forms.
We thank C. Caillarec for having implemented the first steps of the model and F. Nassur for technical help. We are also grateful to A. Cloarec for comments on the manuscript. This work was supported by a grant from the French Ministry of Research and Education to M.L.