Automated tracking and analysis of ant trajectories shows variation in forager exploration

Determining how ant colonies optimize foraging while mitigating pathogen and predator risks provides insight into how the ants have achieved ecological success. Ants must respond to changing resource conditions, but exploration comes at a cost of higher potential exposure to threats. Fungal infected cadavers surround the main foraging trails of the carpenter ant Camponotus rufipes, offering a system to study how foragers behave given the persistent occurrence of disease threats. Studies on social insect foraging behavior typically require many hours of human labor due to the high density of individuals. To overcome this, we developed deep learning based computer vision algorithms to track foraging ants, frame-by-frame, from video footage shot under the natural conditions of a tropical forest floor at night. We found that most foragers walk in straight lines overlapping the same areas as other ants, but there is a subset of foragers with greater exploration. Consistency in walking behavior may protect most ants from infection, while foragers that explore unique portions of the trail may be more likely to encounter fungal spores implying a trade-off between resource discovery and risk avoidance.

[1]  K. Lafferty,et al.  Fear of feces? Tradeoffs between disease risk and foraging drive animal activity around raccoon latrines , 2018 .

[2]  D. Crawford,et al.  Regulation of recruitment by individual scouts inFormica oreas Wheeler (Hymenoptera, Formicidae) , 1983, Insectes Sociaux.

[3]  G. Bard Ermentrout,et al.  Trail following in ants: individual properties determine population behaviour , 1995, Behavioral Ecology and Sociobiology.

[4]  J. J. Howard Costs of trail construction and maintenance in the leaf-cutting ant Atta columbica , 2001, Behavioral Ecology and Sociobiology.

[5]  J. J. Howard,et al.  Conditioning of scouts and recruits during foraging by a leaf-cutting ant, Atta colombica , 1996, Animal Behaviour.

[6]  H. Evans,et al.  Cordyceps species and their anamorphs pathogenic on ants (Formicidae) in tropical forest ecosystems. II: The Camponotus (Formicinae) complex , 1982 .

[7]  Danny Ziyi Chen,et al.  A Matching Model Based on Earth Mover's Distance for Tracking Myxococcus Xanthus , 2014, MICCAI.

[8]  D. Jackson,et al.  U-turns on ant pheromone trails , 2006, Current Biology.

[9]  K. Frisch The dance language and orientation of bees , 1967 .

[10]  K. Del‐Claro,et al.  Ant‐Homoptera Interactions in a Neotropical Savanna: The Honeydew‐Producing Treehopper, Guayaquila xiphias (Membracidae), and its Associated Ant Fauna on Didymopanax vinosum (Araliaceae) 1 , 1999 .

[11]  J. Witte The Ants , 2016 .

[12]  Gwenaël Kaminski,et al.  Individual Experience Alone Can Generate Lasting Division of Labor in Ants , 2007, Current Biology.

[13]  Janice Moore Parasites and the Behavior of Animals , 2002 .

[14]  Lin Yang,et al.  Suggestive Annotation: A Deep Active Learning Framework for Biomedical Image Segmentation , 2017, MICCAI.

[15]  C. Kost,et al.  Spatio-temporal permanence and plasticity of foraging trails in young and mature leaf-cutting ant colonies (Atta spp.) , 2005, Journal of Tropical Ecology.

[16]  T. Seeley Division of labor between scouts and recruits in honeybee foraging , 1983, Behavioral Ecology and Sociobiology.

[17]  I D Couzin,et al.  Self-organized lane formation and optimized traffic flow in army ants , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[18]  David P. Hughes,et al.  Foraging ants trade off further for faster: use of natural bridges and trunk trail permanency in carpenter ants , 2013, Naturwissenschaften.

[19]  J. Boomsma,et al.  Life histories and parasite pressure across the major groups of social insects. , 2005 .

[20]  Donald H. Feener,et al.  Defense against parasites by hitchhikers in leaf-cutting ants: a quantitative assessment , 2004, Behavioral Ecology and Sociobiology.

[21]  K. Jaffe,et al.  On the nestmate-recognition system and territorial marking behaviour in the antCamponotus rufipes , 1984, Insectes Sociaux.

[22]  H. Michael G. Lattorff,et al.  Recognition and Avoidance of Contaminated Flowers by Foraging Bumblebees (Bombus terrestris) , 2011, PloS one.

[23]  Duncan E. Jackson,et al.  Minor workers have a major role in the maintenance of leafcutter ant pheromone trails , 2008, Animal Behaviour.

[24]  D. Hughes,et al.  Long-Term Disease Dynamics for a Specialized Parasite of Ant Societies: A Field Study , 2014, PloS one.

[25]  S. Benhamou How to reliably estimate the tortuosity of an animal's path: straightness, sinuosity, or fractal dimension? , 2004, Journal of theoretical biology.

[26]  Leah Edelstein-Keshet,et al.  Simple models for trail-following behaviour; Trunk trails versus individual foragers , 1994 .

[27]  J. Biesmeijer,et al.  Exploration and exploitation of food sources by social insect colonies: a revision of the scout-recruit concept , 2001, Behavioral Ecology and Sociobiology.

[28]  R. Brandenburg,et al.  Use of Radiography and Tunnel Castings for Observing Mole Cricket (Orthoptera: Gryllotalpidae) Behavior in Soil , 2002 .

[29]  Jean-Louis Deneubourg,et al.  Ant traffic rules , 2010, Journal of Experimental Biology.

[30]  D. Hughes,et al.  Hidden Diversity Behind the Zombie-Ant Fungus Ophiocordyceps unilateralis: Four New Species Described from Carpenter Ants in Minas Gerais, Brazil , 2011, PloS one.

[31]  R. Rae,et al.  Behavioural avoidance by slugs and snails of the parasitic nematode Phasmarhabditis hermaphrodita , 2016 .

[32]  D. Bates,et al.  Fitting Linear Mixed-Effects Models Using lme4 , 2014, 1406.5823.

[33]  F. Ratnieks,et al.  Trail geometry gives polarity to ant foraging networks , 2004, Nature.

[34]  Per B. Brockhoff,et al.  lmerTest Package: Tests in Linear Mixed Effects Models , 2017 .

[35]  C. Carere,et al.  Individual differences in exploratory activity relate to cognitive judgement bias in carpenter ants , 2017, Behavioural Processes.

[36]  T. Seeley The Wisdom of the Hive: The Social Physiology of Honey Bee Colonies , 1995 .

[37]  Kaiming He,et al.  Mask R-CNN , 2017, 2017 IEEE International Conference on Computer Vision (ICCV).

[38]  Marcus Vinícius Vieira,et al.  Indices of movement behaviour: conceptual background, effects of scale and location errors , 2010 .

[39]  J. Deneubourg,et al.  Self-organized shortcuts in the Argentine ant , 1989, Naturwissenschaften.

[40]  Danny Ziyi Chen,et al.  A Hybrid Approach for Segmentation and Tracking of Myxococcus xanthus Swarms. , 2016, IEEE transactions on medical imaging.