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Temporary Prey Storage Along Swarm Columns of Army Ants: an Adaptive Strategy for Successful bioRxiv preprint doi: https://doi.org/10.1101/2021.05.24.445418; this version posted May 26, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder.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. 1 Temporary prey storage along swarm columns of army ants: an adaptive strategy for successful 2 raiding? 3 Hilário Póvoas de Lima1,2, Serafino Teseo3, Raquel Leite Castro de Lima1,2, Ronara Souza Ferreira- 4 Châline1,2, Nicolas Châline1,2 5 1LEEEIS, Laboratory of Ethology, Ecology and Evolution of Insect Societies, Departamento de Psicologia 6 Experimental, Instituto de Psicologia Experimental, Universidade de São Paulo, São Paulo, SP, Brazil 7 2Programa de pós-graduação em Psicologia Experimental, USP, São Paulo, SP, Brazil 8 3School of Biological Sciences, Nanyang Technological University, Singapore 9 10 Keywords: army ants, Eciton, foraging, collective behavior, column raid, cache 11 Abstract 12 While pillaging brood of other social insects, Eciton army ants often accumulate prey in piles (or 13 caches) along their foraging trails. Descriptions scattered throughout the past 100 years link this 14 behavior to foraging-related migration. However, no empirical work has yet investigated its adaptive 15 value. Here we asked whether caches facilitate prey flow from foraging fronts to temporary nests (or 16 bivouacs) in the hook-jawed army ant, Eciton hamatum. We counted workers arriving at caches with 17 prey from foraging fronts and departing caches towards the bivouac, quantifying their prey loads. 18 While more workers carrying single-item prey loads arrived at rather than left caches towards the 19 bivouac, ants carrying multiple-item prey loads arrived at and departed at the same rate. This probably 20 resulted from raiders depositing prey in safe locations and rapidly returning to the foraging front, 21 while other workers safely transported prey to the bivouac in multiple-item loads. This cache- 22 mediated traffic partitioning probably allows maximizing the prey collection rate, and may be a 23 counter-adaptation to the strategies prey colonies deploy to defend their brood from army ants. 24 bioRxiv preprint doi: https://doi.org/10.1101/2021.05.24.445418; this version posted May 26, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder.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. 25 Background 26 In some army ants, cohorts of simultaneously developing larvae require high quantities of protein 27 intake, resulting in bursts of intense foraging activity [1]. Columns of foraging Eciton workers roam 28 neotropical forests in search of prey, often mass-attacking social insect colonies to feed captured 29 brood to their own larvae [2–4]. Insect colonies include large amounts of potential prey, but also 30 adaptively deploy specific defenses against army ant attacks (e.g., coordinated evacuation). This 31 limits the access to prey to relatively short time windows after the beginning of raids [5–14]. 32 Therefore, to maximize prey collection, Eciton raids involve huge numbers of individuals 33 transporting brood from pillaged colonies to their temporary nest (the bivouac) [15]. As many raiding 34 workers travel in both directions along narrow columns, adaptations have emerged that fluidify traffic 35 and minimize risks of bottleneck and traffic congestions. These include multiple-lane trails averting 36 collisions between workers walking opposite directions [16] and ‘living bridges’ of ant bodies over 37 gaps along trails [17]. 38 Despite the presence of traffic-optimizing adaptations, naturalists have frequently observed piles 39 of brood prey (or caches) along the raiding columns of the hook-jawed army ant, E. hamatum. Authors 40 initially suggested that these emerged due to traffic management inefficiencies, as workers going 41 towards the foraging front prevented prey-carrying returning foragers from advancing. According to 42 Schneirla, this ‘virtually forces’ returning raiders ‘to deposit their burdens in piles that form near the 43 places of greatest confusion’ [18]. In the 1950-60’s, Rettenmeyer linked the emergence of caches to 44 the collective dynamics underlying the formation of bivouacs. He suggested that caches form and 45 grow as prey-carrying workers gather in ‘areas of greater booty odor’, eventually leading to the 46 formation of new bivouacs when these reach especially large sizes [19]. Although Rettenmeyer does 47 not explicitly mention it, his observations imply that caches emerge as a result of workers simply 48 depositing prey loads in presence of groups of nestmates with stacked prey. Following this argument, 49 caches were considered as by-products of the same collective dynamics underlying the relocation of 50 bivouacs across novel, potentially prey-rich territories. bioRxiv preprint doi: https://doi.org/10.1101/2021.05.24.445418; this version posted May 26, 2021. 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. 51 Nevertheless, our preliminary work on E. hamatum revealed that prey caches appear regularly at 52 low traffic intensities and at times of the day in which bivouacs are not necessarily relocating. This 53 raises doubts about the hypothesis that prey caches exclusively emerge as a byproduct of bivouac 54 relocation dynamics. In addition, experimental evidence from Atta leaf-cutting ants, which also 55 transport huge quantities of food along long trails, shows that food caches emerge at nest entrances 56 when the inflow of leaf fragments significantly exceeds its processing rate [20,21]. By freeing 57 themselves from their loads, Atta workers readily return to the foraging grounds, maximizing foraging 58 efficiency. This corroborates the idea that food caches can have an adaptive function in E. hamatum. 59 We therefore hypothesized that caches allow optimizing the transport of prey from the foraging fronts 60 to the bivouac. To test this hypothesis, we measured the traffic of workers approaching caches from 61 the foraging front and returning to the bivouac, assessing the quantity of prey each worker transported. 62 Methods 63 Cache collection and prey characterization 64 We carried out the research in a 220 ha area of an Amazonian primary forest fragment (Terra 65 Firme, coordinates: -1.034113, -46.766017) in the Bragança city area, state of Pará, Brazil. To locate 66 E. hamatum caches, we searched for and followed foraging columns across multiple experimental 67 sessions (July 2019-January 2020) between 8:00 am and 4:30 pm, when E. hamatum forages [22]. 68 We identified caches as structures including stacked prey brood and stationary E. hamatum workers 69 (Figure 1A), as well as workers approaching and leaving the area. To minimize the likelihood of 70 resampling the same colony, we did not collect caches in predation events closer than 50 meters. For 71 each cache, we first inspected the surrounding 10-meter radius for prey nests or bivouacs; then, we 72 noted whether caches appeared at multiple-trail junctions, whether they were exposed or covered by 73 leaf litter/fallen tree branches and if they were at the side of - or crossed by - trails. Finally, we 74 assessed if debris or other structures slowed down the worker flow in the respective trails. Where 75 possible, we collected all prey from easily accessible caches in a single quick move. We immediately 76 placed collected caches in 700 ml plastic containers, storing ant prey sorted by developmental stages bioRxiv preprint doi: https://doi.org/10.1101/2021.05.24.445418; this version posted May 26, 2021. 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. 77 (larva, pupa, adult) in 70% ethanol. We later identified prey at the subfamily/genus level using keys 78 for neotropical adult ants [23] ⁠ and larvae [24] , and measured their length. 79 Worker flow 80 We filmed caches for 5 minutes from approximately 30 cm of height at 30 fps and 1920 x 1080px. 81 The frame included portions of worker columns, with individuals arriving from the foraging front to 82 the cache and leaving towards the bivouac, as well as individuals passing at the side of the cache, that 83 were considered part of the same trail. Assuming that E. hamatum workers only transport prey from 84 the foraging front to the cache to the bivouac, and not the contrary, we established a region between 85 the foraging front and the cache (RFC), and a region between the cache and the bivouac (RCB) 86 (Figure 1D). We counted workers passing through the cache via RFC and RCB, in both directions, 87 noting if they carried one, multiple or no prey items (Figure 1B, C). We visually analyzed each video 88 using the software Boris [25]. bioRxiv preprint doi: https://doi.org/10.1101/2021.05.24.445418; this version posted May 26, 2021. 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. 89 90 Figure 1. A. Eciton hamatum cache on a dry leaf (primary rainforest floor, Bragança, Pará, Brazil). 91 B. Worker carrying two prey items. C. Worker carrying a single prey item. D. The flow of ants 92 passing through caches. RFC: region between the foraging front and the cache; RCB: region between 93 the cache and the bivouac. Foraging workers travel along two lanes with opposite directions. 94 Statistics 95 We compared numbers of workers walking in the same direction going through RCB and RFC, 96 considering these as paired data, with Wilcoxon signed-rank tests. We conducted separate tests for 97 workers carrying one, multiple or no prey items. For analyses of workers walking in both directions, 98 we considered data as unpaired, and used the Mann Whitney U test.
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