Memory, not just perception, plays an important role in terrestrial mammalian migration

One of the key questions regarding the underlying mechanisms of mammalian land migrations is how animals select where to go. Most studies assume perception of resources as the navigational mechanism. The possible role of memory that would allow forecasting conditions at distant locations and times based on information about environmental conditions from previous years has been little studied. We study migrating zebra in Botswana using an individual-based simulation model, where perceptually guided individuals use currently sensed resources at different perceptual ranges, while memory-guided individuals use long-term averages of past resources to forecast future conditions. We compare simulated individuals guided by perception or memory on resource landscapes of remotely sensed vegetation data to trajectories of GPS-tagged zebras. Our results show that memory provides a clear signal that best directs migrants to their destination compared to perception at even the largest perceptual ranges. Zebras modelled with memory arrived two to four times, or up to 100 km, closer to the migration destination than those using perception. We suggest that memory in addition to perception is important for directing ungulate migration. Furthermore, our findings are important for the conservation of migratory mammals, as memory informing direction suggests migration routes could be relatively inflexible.

[1]  P. Berthold,et al.  Migratory orientation of first-year white storks (Ciconia ciconia): inherited information and social interactions , 2004, Journal of Experimental Biology.

[2]  Jarrett J. Barber,et al.  Quantifying ecological memory in plant and ecosystem processes. , 2015, Ecology letters.

[3]  William F. Fagan,et al.  Search and navigation in dynamic environments – from individual behaviors to population distributions , 2008 .

[4]  Simon Benhamou,et al.  Spatial memory and animal movement. , 2013, Ecology letters.

[5]  E. Milner‐Gulland,et al.  Tracking greenery across a latitudinal gradient in central Asia – the migration of the saiga antelope , 2010 .

[6]  J. Polovina.  Decadal variation in the trans-Pacific migration of northern bluefin tuna (Thunnus thynnus) coherent with climate-induced change in prey abundance , 1996 .

[7]  Andrew K. Skidmore,et al.  Displaying remotely sensed vegetation dynamics along natural gradients for ecological studies , 2008 .

[8]  Daniel I Rubenstein,et al.  Correction for Giuggioli et al., Stigmergy, collective actions, and animal social spacing , 2016, Proceedings of the National Academy of Sciences.

[9]  M. E. Nelson,et al.  Development of migratory behavior in northern white-tailed deer , 1998 .

[10]  Wolfgang Wiltschko,et al.  Avian navigation: from historical to modern concepts , 2003, Animal Behaviour.

[11]  Hall Sawyer,et al.  Stopover ecology of a migratory ungulate. , 2011, The Journal of animal ecology.

[12]  J. Berger,et al.  Connecting the dots: an invariant migration corridor links the Holocene to the present , 2006, Biology Letters.

[13]  A. Huete,et al.  Overview of the radiometric and biophysical performance of the MODIS vegetation indices , 2002 .

[14]  Atle Mysterud,et al.  A Migratory Northern Ungulate in the Pursuit of Spring: Jumping or Surfing the Green Wave? , 2012, The American Naturalist.

[15]  P. Berthold,et al.  Quantitative genetic analysis of migratory behaviour , 2003 .

[16]  Ryan M. Nielson,et al.  A framework for understanding semi-permeable barrier effects on migratory ungulates , 2013 .

[17]  E. Laca,et al.  Mechanisms that result in large herbivore grazing distribution patterns. , 1996 .

[18]  Clément Calenge,et al.  The package “adehabitat” for the R software: A tool for the analysis of space and habitat use by animals , 2006 .

[19]  C. Mettke-Hofmann,et al.  Long-term memory for a life on the move , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[20]  L. Talbot,et al.  WILDLIFE MONOGRAPHS. THE WILDEBEEST IN WESTERN MASAILAND, EAST AFRICA, , 1963 .

[21]  Matthew G. Betts,et al.  Dynamic occupancy models reveal within-breeding season movement up a habitat quality gradient by a migratory songbird , 2008 .

[22]  John M. Fryxell,et al.  Opposing Rainfall and Plant Nutritional Gradients Best Explain the Wildebeest Migration in the Serengeti , 2009, The American Naturalist.

[23]  Jacqui Frair,et al.  The attraction of the known: the importance of spatial familiarity in habitat selection in wapiti Cervus elaphus , 2009 .

[24]  S. McNaughton,et al.  Grazing as an Optimization Process: Grass-Ungulate Relationships in the Serengeti , 1979, The American Naturalist.

[25]  E. Laca.  Spatial memory and food searching mechanisms of cattle , 1998 .

[26]  Volker Grimm,et al.  Integrating individual search and navigation behaviors in mechanistic movement models , 2011, Theoretical Ecology.

[27]  Birgit Müller,et al.  A standard protocol for describing individual-based and agent-based models , 2006 .

[28]  James J. Anderson,et al.  Modeling climate change impacts on phenology and population dynamics of migratory marine species , 2013 .

[29]  C. Brooks,et al.  Directed movement and orientation across a large natural landscape by zebras, Equus burchelli antiquorum , 2008, Animal Behaviour.

[30]  J. McNamara,et al.  Animal migration: linking models and data beyond taxonomic limits , 2009, Biology Letters.

[31]  Melissa S. Bowlin,et al.  Grand Challenges in Migration Biology , 2010, Integrative and comparative biology.

[32]  Gil Bohrer,et al.  Elephant movement closely tracks precipitation-driven vegetation dynamics in a Kenyan forest-savanna landscape , 2014, Movement ecology.

[33]  Benjamin D. Dalziel,et al.  Fitting Probability Distributions to Animal Movement Trajectories: Using Artificial Neural Networks to Link Distance, Resources, and Memory , 2008, The American Naturalist.

[34]  Michelle E. Gadd,et al.  Barriers, the Beef Industry and Unnatural Selection: A Review of the Impact of Veterinary Fencing on Mammals in Southern Africa , 2012 .

[35]  Markus Ahola,et al.  Variation in climate warming along the migration route uncouples arrival and breeding dates , 2004 .

[36]  Allison K. Shaw,et al.  Migration or Residency? The Evolution of Movement Behavior and Information Usage in Seasonal Environments , 2012, The American Naturalist.

[37]  M. E. Miller,et al.  The Trappers Point Site (48SU1006): Early Archaic Adaptations and Pronghorn Procurement in the Upper Green River Basin, Wyoming , 2000, Plains anthropologist.

[38]  J. Berger,et al.  Global decline in aggregated migrations of large terrestrial mammals , 2009 .

[39]  John F. Wilmshurst,et al.  PREDICTIVE MODELS OF MOVEMENT BY SERENGETI GRAZERS , 2004 .

[40]  L. Talbot,et al.  The wildebeest in Western Masailand, East Africa. , 1963 .

[41]  Susanne Akesson,et al.  The genetics of migration on the move. , 2011, Trends in ecology & evolution.

[42]  Bertrand Dumont,et al.  Response of foraging sheep to variability in the spatial distribution of resources , 2005, Animal Behaviour.

[43]  J. Gareth Polhill,et al.  The ODD protocol: A review and first update , 2010, Ecological Modelling.

[44]  Garrett M. Street,et al.  On the adaptive benefits of mammal migration , 2014 .

[45]  William F Fagan,et al.  Transient windows for connectivity in a changing world , 2014, Movement Ecology.

[46]  D. Doak,et al.  The need for integrative approaches to understand and conserve migratory ungulates. , 2007, Ecology letters.

[47]  S. Levin,et al.  Stigmergy, collective actions, and animal social spacing , 2013, Proceedings of the National Academy of Sciences.

[48]  J. Hopcraft,et al.  Serengeti wildebeest migratory patterns modeled from rainfall and new vegetation growth. , 2006, Ecology.

[49]  J. Giske,et al.  Cues and decision rules in animal migration , 2011 .

[50]  Martin Wikelski,et al.  Going, Going, Gone: Is Animal Migration Disappearing , 2008, PLoS biology.

[51]  Brian Huntley,et al.  Travelling through a warming world: climate change and migratory species. , 2009 .

[52]  Garry D. Peterson.  Contagious Disturbance, Ecological Memory, and the Emergence of Landscape Pattern , 2002, Ecosystems.

[53]  N. Pettorelli,et al.  The Normalized Difference Vegetation Index (NDVI): unforeseen successes in animal ecology , 2011 .

[54]  S. Harris,et al.  Will reconnecting ecosystems allow long-distance mammal migrations to resume? A case study of a zebra Equus burchelli migration in Botswana , 2011, Oryx.

[55]  Chloe Bracis,et al.  Memory Effects on Movement Behavior in Animal Foraging , 2015, PloS one.

[56]  R. Drent,et al.  Balancing the energy budgets of arctic-breeding geese through- out the annual cycle: a progress report , 1978 .

[57]  Mark Hebblewhite,et al.  A MULTI-SCALE TEST OF THE FORAGE MATURATION HYPOTHESIS IN A PARTIALLY MIGRATORY UNGULATE POPULATION , 2008 .

[58]  D. Ainley,et al.  Migration routes of sooty shearwaters in the Pacific ocean , 1999 .

[59]  Garrett M. Street,et al.  Space-use behaviour of woodland caribou based on a cognitive movement model. , 2015, The Journal of animal ecology.

[60]  Gil Bohrer,et al.  In search of greener pastures: Using satellite images to predict the effects of environmental change on zebra migration , 2013 .

[61]  Xiao-Hua Zhou,et al.  Statistical Methods for Meta‐Analysis , 2008 .

[62]  E. F. Baerwald,et al.  Are migratory behaviours of bats socially transmitted? , 2016, Royal Society Open Science.