bioRxiv preprint doi: https://doi.org/10.1101/194100; this version posted September 28, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. Behavioral diversity assisting obstacle navigation during group transportation in ant Shohei Utsunomiya1, Atsuko Takamatsu1* 1 Department of Electrical Engineering and Bioscience, Waseda University, Shinjuku-ku, Tokyo 169-8555, Japan * atsuko [email protected] Abstract Cooperative transportation behavior in ants has attracted attention from a wide range of researchers, from behavioral biologists to roboticists. Ants can accomplish complex tasks as a group whereas individual ants are not intelligent (in the context of this study's tasks). In this study, group transportation and obstacle navigation in Formica japonica, an ant species exhibiting `uncoordinated transportation' (primitive group transportation), are observed using two differently conditioned colonies. Analyses focus on the effect of group size on two key quantities: transportation speed and obstacle navigation period. Additionally, this study examines how these relationships differ between colonies. The tendencies in transportation speed differ between colonies whereas the obstacle navigation period is consistently reduced irrespective of the colony. To explain this seemingly inconsistent result in transportation speed, we focus on behavioral diversity in `directivity', defined as the tendency of individual ants to transport a food item toward their own preferential direction. Directivity is not always toward the nest, but rather is distributed around it. The diversity of the first colony is less than that of the second colony. Based on the above results, a mechanical model is constructed. Using the translational and rotational motion equations of a rigid rod, the model mimics a food item being pulled by single or multiple ants. The directions of pulling forces exerted by individual ants are assumed to be distributed around the direction pointing toward the nest. The simulation results suggest that, as diversity in directivity increases, so does the success rate in more complicated obstacle navigation. In contrast, depending on group size, the speed of group transportation increases in the case of lower diversity while it is almost constant in the case of higher diversity. Transportation speed and obstacle navigation success rate are in a trade-off relationship. Author summary Cooperative transportation behavior in ants attracts researchers from behavioral biologists to roboticists. Ants can accomplish complex tasks in groups, whereas individuals are not likely intelligent. Recent reports focus on higher-level mechanisms in coordinated transportation, e.g., triggering by an informed ant. In contrast, this study focuses on the simplest form of group transportation where there is no specialist in the group. We analyze group transportation and obstacle navigation combined with mechanical model analysis. Behavioral diversity in `directivity' is found to govern performance effectiveness. Here, directivity is defined as the tendency of an individual 1/17 bioRxiv preprint doi: https://doi.org/10.1101/194100; this version posted September 28, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. ant to preferentially transport a food item in its own direction rather than in the nest direction. Such outliers can impede transportation speed but contribute well to the system when a group of ants is hindered by a complex obstacle. It is noteworthy that the two measures of efficiency, transportation speed and success rate of obstacle navigation, are in a trade-off relationship. Introduction 1 Fully coordinated systems are fragile because, once a part of the system becomes 2 unstable, the whole system can sometimes cease to function. In contrast, a fully 3 decentralized system consisting of simple elements can work well even if some elements 4 are broken. Group transportation in ants is a good example of such a decentralized 5 system. Although individual ants are not intelligent in the context of this study ’s 6 tasks, they can accomplish complex tasks through local interaction, sometimes even 7 without a leader. Consequently, researchers from fields as diverse as behavioral 8 biology, physics, and robotics have studied group transportation in ants [1{7]. In 9 contrast, quantitative analysis of group transportation behavior has been insufficient 10 until recently. 11 Group transportation is a behavior in which two or more worker ants move a large 12 food item that not transportable by a single ant. The behavior was categorized into 13 three kinds or transportation by Czaczkes and Ratnieks: uncoordinated, encircling 14 coordinated, and forward-facing cooperative [1]. In uncoordinated transportation, ants 15 pull a food item in opposite directions [8], resulting in slow-speed transportation 16 and/or frequently reaching a deadlock. In encircling coordinated transportation, ants 17 encircle a food item and the majority of members align at the side of the moving front 18 and pull it, whereas minor members align at the back and pull, lift, or push it. This 19 behavior achieves quick transportation, rarely reaching a deadlock. In forward-facing 20 cooperative transportation, a leader ant lifts the food item as its head faces forward 21 while smaller ants subsequently join behind the leader to stabilize the transportation 22 of the item [9]. In the last case, the role and appearance of each ant are clearly 23 distinct; thus, it is out of scope in this study. Uncoordinated transportation has been 24 categorized by McCreery and Breed [10] as transportation without `information 25 transfer,' and the latter two as transportation with `information transfer. ’ 26 Recently, encircling coordinated transportation or transportation with information 27 transfer has been investigated intensively in cases where worker ants appear indistinct 28 but have roles that seem to be different during transportation. The workers of the 29 longhorn crazy ant, Paratrechina longicornis, exhibit fluctuating motion during group 30 transportation. However, they switch to straight movement when closer to the nest 31 once a single informed ant, possessing information on the direction of the nest, attaches 32 itself to the group [3]. Furthermore, this species exhibits excellent performance during 33 obstacle navigation, switching its behavior intrinsically without the attachment of an 34 informed ant [11]. Moreover, under imposition of a constraint such as an obstacle 35 barrier, oscillatory group motion emerges which assists in navigating the obstacle [12]. 36 To achieve the above higher-level strategies for group transportation and obstacle 37 navigation, sophisticated mechanisms are required. In contrast, this study focuses on a 38 lower-level but very simple strategy. By observing the behavior of Japanese wood 39 ants, Formica japonica, the fundamental problem emerging through local interaction 40 was investigated, where individual worker ants follow a simple rule and interact 41 through the food item according to kinematics. 42 The ants, F. japonica are widely distributed in Japan [13,14] and have been 43 investigated particularly with regard to landmark navigation [15], social 44 interaction [16,17], etc. Most ants of this species lives under open ground and 45 2/17 bioRxiv preprint doi: https://doi.org/10.1101/194100; this version posted September 28, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. transport large food items in groups without dissection [18]. During group 46 transportation, the ants pull the food item in their own preferential directions (Fig 1); 47 Some pull the item toward their nest (denoted by a black arrowhead) and others pull 48 it in the opposite direction of the nest (denoted by a white arrowhead). This results in 49 tug-of-war movement (S1 Video). Thus, their manner of transportation could be 50 categorized as `uncoordinated' [1] and this species has been believed to exhibit 51 low-efficiency transportation [1,8,10]. This is, however, a good model animal for 52 investigating how the lowest-level strategy can solve tasks using simple rules. We show 53 that the key mechanism is behavioral diversity in `directivity, ’which is defined as the 54 tendency of an individual ant to transport a food item in its own preferential 55 direction. How diversity in directivity supports obstacle navigation is discussed. 56 Fig 1. Tug of war observed in ants, Formica japonica, transporting a food item. (A{C) are arranged chronologically in 1-s intervals. The arrow indicates the direction of the nest. The ant denoted by the black arrowheads attempts to drag the food item toward the nest while the ant denoted by the white arrowheads acts against it, resulting in moving the food item in the opposite direction from the nest. See also S1 Video. Results 57 The behavior of F. japonica ants during group transportation of a food item toward 58 their nest and their obstacle navigation were observed on a stage placed in an indoor 59 artificial environment termed colony (I), or in the outdoor natural environment termed 60 colony (II) (Fig 2; See the Materials and Method section for details). Then the 61 transportation speed, obstacle-passing period, and direction of transportation were 62 analyzed. 63 In individual transportation, ants moved the food items, which were 5{10 times 64 longer and 20 times heavier than a worker ant, by pulling them. During long periods of 65 group transportation with two or more members, the composition of the members was 66 dynamically substituted as reported in the above literature [3,11,19]. This behavior 67 can cause randomness, fluctuating behavior, and/or `information transfer' into the 68 group by newly attached ants. In contrast, in this study only cases of fixed member 69 composition were analyzed because we focused on the basic level of group behavior. 70 Fig 2. Experimental setup. (A) Setup for observation.