Collective foraging in spatially complex nutritional environments

Nutrition impinges on virtually all aspects of an animal's life, including social interactions. Recent advances in nutritional ecology show how social animals often trade-off individual nutrition and group cohesion when foraging in simplified experimental environments. Here, we explore how the spatial structure of the nutritional landscape influences these complex collective foraging dynamics in ecologically realistic environments. We introduce an individual-based model integrating key concepts of nutritional geometry, collective animal behaviour and spatial ecology to study the nutritional behaviour of animal groups in large heterogeneous environments containing foods with different abundance, patchiness and nutritional composition. Simulations show that the spatial distribution of foods constrains the ability of individuals to balance their nutrient intake, the lowest performance being attained in environments with small isolated patches of nutritionally complementary foods. Social interactions improve individual regulatory performances when food is scarce and clumpy, but not when it is abundant and scattered, suggesting that collective foraging is favoured in some environments only. These social effects are further amplified if foragers adopt flexible search strategies based on their individual nutritional state. Our model provides a conceptual and predictive framework for developing new empirically testable hypotheses in the emerging field of social nutrition. This article is part of the themed issue ‘Physiological determinants of social behaviour in animals’.

[1]  I. Couzin,et al.  Collective memory and spatial sorting in animal groups. , 2002, Journal of theoretical biology.

[2]  Mathieu Lihoreau,et al.  Recent advances in the integrative nutrition of arthropods. , 2015, Annual review of entomology.

[3]  C. Grüter,et al.  Insights from insects about adaptive social information use. , 2014, Trends in ecology & evolution.

[4]  Iain D. Couzin Collective animal behaviour. , 1999 .

[5]  S. Behmer Insect herbivore nutrient regulation. , 2009, Annual review of entomology.

[6]  Michael H. Dickinson,et al.  Automated monitoring and quantitative analysis of feeding behaviour in Drosophila , 2014, Nature Communications.

[7]  Michael A Charleston,et al.  Nutritional ecology beyond the individual: a conceptual framework for integrating nutrition and social interactions , 2015, Ecology letters.

[8]  N. Dingemanse,et al.  Individuality in nutritional preferences: a multi-level approach in field crickets , 2016, Scientific Reports.

[9]  Vicsek,et al.  Novel type of phase transition in a system of self-driven particles. , 1995, Physical review letters.

[10]  Donald S. Fussell,et al.  Computer rendering of stochastic models , 1982, Commun. ACM.

[11]  R. Sibly,et al.  Optimal foraging when regulating intake of multiple nutrients , 2004, Animal Behaviour.

[12]  T. Collett,et al.  Spatial Memory in Insect Navigation , 2013, Current Biology.

[13]  David Raubenheimer,et al.  Sex-Specific Fitness Effects of Nutrient Intake on Reproduction and Lifespan , 2008, Current Biology.

[14]  A. M. Edwards,et al.  Revisiting Lévy flight search patterns of wandering albatrosses, bumblebees and deer , 2007, Nature.

[15]  Alistair M. Senior,et al.  Social Network Analysis and Nutritional Behavior: An Integrated Modeling Approach , 2016, Front. Psychol..

[16]  D. Ingram,et al.  Activity Measures in Rhesus Monkeys on Long-Term Calorie Restriction , 1997, Physiology & Behavior.

[17]  I. Couzin,et al.  Cannibal crickets on a forced march for protein and salt. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[18]  B. Rogina,et al.  Behavioral, physical, and demographic changes in Drosophila populations through dietary restriction , 2005, Aging cell.

[19]  Shinichi Nakagawa,et al.  An Overlooked Consequence of Dietary Mixing: A Varied Diet Reduces Interindividual Variance in Fitness , 2015, The American Naturalist.

[20]  S. Simpson,et al.  Macronutrient balance, reproductive function, and lifespan in aging mice , 2015, Proceedings of the National Academy of Sciences.

[21]  D C Krakauer,et al.  Spatial scales of desert locust gregarization. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[22]  J. Deneubourg,et al.  Group personality during collective decision-making: a multi-level approach , 2015, Proceedings of the Royal Society B: Biological Sciences.

[23]  Jérôme Buhl,et al.  Evolving Nutritional Strategies in the Presence of Competition: A Geometric Agent-Based Model , 2015, PLoS Comput. Biol..

[24]  David Raubenheimer,et al.  Putting the Balance Back in Diet , 2015, Cell.

[25]  M. Lihoreau,et al.  Adaptive collective foraging in groups with conflicting nutritional needs , 2016, Royal Society Open Science.

[26]  Stefan Krause,et al.  Swarm intelligence in animals and humans. , 2010, Trends in ecology & evolution.

[27]  S. Shafir,et al.  Honey bee foragers balance colony nutritional deficiencies , 2016, Behavioral Ecology and Sociobiology.

[28]  David Raubenheimer,et al.  The Nature of Nutrition: A Unifying Framework from Animal Adaptation to Human Obesity , 2012 .

[29]  Steven C. Cook,et al.  Colony-level macronutrient regulation in ants: mechanisms, hoarding and associated costs , 2010, Animal Behaviour.

[30]  Denis Réale,et al.  Behavioural reaction norms: animal personality meets individual plasticity. , 2010, Trends in ecology & evolution.

[31]  Stephen J. Simpson,et al.  Predator Percolation, Insect Outbreaks, and Phase Polyphenism , 2009, Current Biology.

[32]  A. Dornhaus,et al.  Benefits of recruitment in honey bees: effects of ecology and colony size in an individual-based model , 2006 .

[33]  S. Altizer,et al.  Dynamics of macronutrient self-medication and illness-induced anorexia in virally infected insects , 2013, The Journal of animal ecology.

[34]  I. Couzin,et al.  Emergent Sensing of Complex Environments by Mobile Animal Groups , 2013, Science.

[35]  Jonathan Wright Foraging: Behavior and Ecology, David W. Stephens, Joel S. Brown, Ronald C. Ydenberg (Eds.). University of Chicago Press, Chicago (2007), Pp. xiii+608. Price £23.50 paperback , 2008 .

[36]  Uzi Motro,et al.  NEAR-FAR SEARCH : AN EVOLUTIONARILY STABLE FORAGING STRATEGY , 1995 .

[37]  Pawel Romanczuk,et al.  Nutritional state and collective motion: from individuals to mass migration , 2011, Proceedings of the Royal Society B: Biological Sciences.

[38]  S. Simpson,et al.  Modelling nutritional interactions: from individuals to communities. , 2010, Trends in ecology & evolution.

[39]  Christian A. Yates,et al.  Inherent noise can facilitate coherence in collective swarm motion , 2009, Proceedings of the National Academy of Sciences.

[40]  Damien R. Farine,et al.  Individual-level personality influences social foraging and collective behaviour in wild birds , 2014, Proceedings of the Royal Society B: Biological Sciences.

[41]  Kyung-Jin Min,et al.  Sexual dimorphism in nutrient intake and life span is mediated by mating in Drosophila melanogaster , 2013, Animal Behaviour.

[42]  David Raubenheimer,et al.  Lifespan and reproduction in Drosophila: New insights from nutritional geometry , 2008, Proceedings of the National Academy of Sciences.

[43]  Sasha R. X. Dall,et al.  Information and its use by animals in evolutionary ecology. , 2005, Trends in ecology & evolution.

[44]  T. Valone,et al.  Public Information: From Nosy Neighbors to Cultural Evolution , 2004, Science.

[45]  T. Caraco,et al.  Social Foraging Theory , 2018 .

[46]  S. Wilder,et al.  Spider Nutrition: An Integrative Perspective , 2011 .

[47]  David Raubenheimer,et al.  Match and mismatch: conservation physiology, nutritional ecology and the timescales of biological adaptation , 2012, Philosophical Transactions of the Royal Society B: Biological Sciences.

[48]  Gregory P. Brown,et al.  An evolutionary process that assembles phenotypes through space rather than through time , 2011, Proceedings of the National Academy of Sciences.

[49]  I. Couzin Collective minds , 2007, Nature.

[50]  David Raubenheimer,et al.  A multi-level analysis of feeding behaviour: the geometry of nutritional decisions , 1993 .

[51]  Pietro Perona,et al.  Automated image-based tracking and its application in ecology. , 2014, Trends in ecology & evolution.

[52]  D. Mortensen,et al.  Macronutrient ratios in pollen shape bumble bee (Bombus impatiens) foraging strategies and floral preferences , 2016, Proceedings of the National Academy of Sciences.

[53]  Audrey Dussutour,et al.  Communal Nutrition in Ants , 2009, Current Biology.

[54]  C. Chapman,et al.  Nutritional geometry: gorillas prioritize non-protein energy while consuming surplus protein , 2011, Biology Letters.

[55]  David Raubenheimer,et al.  Food distance and its effect on nutrient balancing in a mobile insect herbivore , 2003, Animal Behaviour.

[56]  R. Sibly,et al.  Producers and scroungers: A general model and its application to captive flocks of house sparrows , 1981, Animal Behaviour.

[57]  I. Couzin,et al.  Shared decision-making drives collective movement in wild baboons , 2015, Science.

[58]  K. Knight A comparative perspective on epigenetics , 2015, Journal of Experimental Biology.

[59]  S. J. Simpson,et al.  The role of food distribution and nutritional quality in behavioural phase change in the desert locust , 2000, Animal Behaviour.

[60]  Michael A Charleston,et al.  Modelling nutrition across organizational levels: from individuals to superorganisms. , 2014, Journal of insect physiology.