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Navigation: from animal behaviour to guiding principles

BY KATHRYN KNIGHT at Journal of Experimental Biology

Whether an animal’s world is restricted to a few twigs or the avian highways that traverse the planet, creatures must navigate their surroundings with every fin stroke, wing beat and stride. ‘Navigation is one of the basic problems that almost all mobile animals, including ourselves, have to solve’, says JEB Editor Almut Kelber from the University of Lund, Sweden. Humans have been fascinated by animals’ navigational abilities for centuries. In recent years, scientists have begun unravelling the mysteries of navigation on grand and small scales, to reveal the mechanisms that allow some to determine their direction of travel, the distances that they must cover and the sensory systems that guide them. However, Kelber explains that the concepts and techniques used by the communities that study animal navigation in organisms from insects to mammals vary significantly, and there is little discussion between these groups. Excited by the prospects offered by recently developed techniques, which will allow scientists to identify the essential genes and neural circuits that control navigation, Kelber has compiled a collection of inspirational Review articles, which discuss navigational behaviours, sensory guidance systems and the mechanisms that allow animals to maintain a sense of location and set a bearing.

Animals and their maps

‘I wanted to bring together work that really describes animal behaviour in detail’, says Kelber, who invited Russell Wyeth from St Francis Xavier University, Canada, to review what is currently known about navigation in aquatic gastropods (jeb185843). Guided by a wide range of senses, the slowly moving creatures frequently pursue odours in search of food and mates, in addition to fleeing the scent of predators. Explaining how the molluscs might follow attractive odours – either by moving in the direction of the water flow carrying the odour, or by moving toward the position where the odour is strongest – Wyeth outlines the circuitry that guides gastropods; from the sensory neurons that detect scents to the motor neurons that drive their movements and the control circuits that determine when the animals turn.

While a keen sense of smell is essential for gastropods in search of food, Gabriele Gerlach from the University of Oldenburg, Germany, and colleagues describe how larval reef fish also follow their sense of smell when returning home, after having been washed out to sea (jeb189746). As it currently is not possible to investigate the neural mechanisms that allow reef fish to navigate home, the team has switched focus to the better-understood zebrafish. They discovered that 6-day-old zebrafish larvae must be able to see each other to learn to associate the scent of the water with their siblings, the presence of which indicates that they are ‘home’. It seems that the larvae also learn to sniff out a specific class of proteins produced by the immune system – major histocompatibility complex proteins – to identify related fish that also define home. Gerlach then outlines evidence supporting the possibility that crypt cells, a type of nerve cell that contributes to scent recognition in other species, may be involved in zebrafish and reef fish homing.

Loggerhead sea turtle (Caretta caretta) hatchlings.
Loggerhead sea turtle (Caretta caretta) hatchlings. Photo credit: Kenneth Lohmann.

However, the scale of the challenge faced by returning reef fish pales into insignificance alongside the ocean-wide odysseys upon which sea turtles and salmon embark. Kenneth and Catherine Lohmann from the University of North Carolina, USA, explain that adult turtles and salmon navigate back to their area of origin predominantly using a magnetic sense, adjusting their bearings as they voyage across oceans by detecting subtle differences in the geomagnetic field (jeb184077). While salmon resort to following their sense of smell during the final approach to their spawning grounds, female turtles locate their home beaches by seeking out the magnetic signature that distinguishes their nesting beach from others.

Moving on from the challenge of long-distance aquatic navigation, Barbara Webb from the University of Edinburgh, UK, reviews some of the impressive breakthroughs that have been made recently in our understanding of the navigation mechanisms used by insects such as ants and bees (jeb188094). Webb describes developing a powerful mathematical model that accurately reproduces the insects’ navigational powers based on three factors: their ability to return home directly after following a circuitous outbound path (known as path integration); their ability to memorize the position of significant locations, such as food sites, and subsequently use the memory to return to those locations; and a visual memory of the surrounding area, which the insect matches with its current view, to maintain its course. Although she warns that this model does not explain all aspects of the insects’ extraordinary navigational abilities, Webb has used the insect-inspired strategy to design successful robot guidance systems.

While ants and bees cover great distances during daily foraging excursions, their ventures are on a far smaller scale than the annual migrations undertaken by some insects and birds. Focusing on the European blackcap and North American monarch butterfly populations, both of which perform migrations over hundreds and thousands of kilometres, Christine Merlin from Texas A&M University, USA, and Miriam Liedvogel from the Max Planck Institute for Evolutionary Biology, Germany, explain that we are beginning to learn more about the genetics of long-distance navigation (jeb191890). They review how a significant proportion of the differences in the migratory strategies used by distinct blackcap populations can be attributed to their genetic differences, while the expression of specific genes, which are epigenetically regulated, accounts for the monarch butterflies’ intergenerational migration. They add that the use of novel genetic techniques is revolutionising our understanding of navigation and will allow researchers to identify key genes and regulatory pathways modulating these extraordinary odysseys.

A simulation of a person walking through a virtual reality maze.
A simulation of a person walking through a virtual reality maze. Photo credit: William Warren.

Considering the mechanism that humans use to negotiate their environment, William Warren from Brown University, USA, blows apart the conventional myth that humans navigate according to a traditional map carried in the head (jeb187971). Describing experiments based on a virtual reality maze linking eight locations that participants could explore, Warren explains that the maze included an impossible twist – two ‘wormholes’ between remote positions in the maze – allowing him to essentially teleport volunteers to a new location and rotate them by 90 deg. Surprisingly, the participants were completely unaware of the relocation, yet when asked to take shortcuts in a subsequent test, they exploited the wormholes. Based on this behaviour, Warren suggests that we perceive the world as a ‘network of paths between places that are augmented with local metric information’, and he explains that his strategy allows us to find new routes to familiar locations, make successful detours, and even take rough shortcuts.

Technical developments

Tagged Egyptian fruit bats (Rousettus aegyptiacus).
Tagged Egyptian fruit bats (Rousettus aegyptiacus). Photo credit: Michal Samuni.

Although many species depend on a range of familiar senses for navigation, other creatures depend on senses that are completely alien to us. Emerging from their roosts after dark, bats use ultrasound cries for high-precision navigation, hunting and communication. Yossi Yovel and Stefan Greif from Tel Aviv University, Israel, review how recent developments in miniature tag design now make it possible for researchers to eavesdrop directly on the echolocation calls of bats while simultaneously recording their behaviour (jeb184689). They outline what we can learn about the navigation strategies of other animals, their diets and how they forage, as well as social interactions and communication using on-board technology. In addition, they suggest that tagged animals could spy on other species, allowing researchers to learn about animals that would otherwise be impossible to investigate, exploiting acoustic information to glean information about their movements, the environment that they are moving through and even their breath rate.

In another technological breakthrough, Nadine Diersch and Thomas Wolbers, from the German Centre for Neurodegenerative Diseases, review how virtual reality is helping us to understand the loss of spatial awareness that accompanies neurodegenerative disease and ageing in humans and rodents (jeb187252). They say that virtual reality simulations allow researchers to create realistic environments while tracking the movements and reactions of volunteers moving through situations that would be impossible in the real world. However, they warn that there are drawbacks to the use of virtual reality when working with the elderly. These include the lack of additional physical cues – such as information about the position of an individual’s body in space – which may alter the participant’s perceptions and behaviour, as well as the increased risk of cyber sickness in older people, who are often less familiar with virtual reality technology.

Neural control of navigation

Shifting focus from navigational behaviour to the neural systems that integrate sensory information to guide navigation, Kelber says, ‘Animals are not machines, so their navigation mechanisms are not designed by engineers, but have been evolved over millions of years in a changing world. I find it highly fascinating how such systems function’.

Introducing us to the central complex, the region of the brain that controls navigational behaviour in insects, Stanley Heinze and colleagues from Lund University, Sweden, explain that the structure has remained virtually unchanged for 400 million years. Collating sensory inputs from the antennae, wings and visual system, the central complex integrates this with information about the position of objects in the sky, such as the sun or moon – which are distant and can function as a compass – allowing animals to take a bearing (jeb188854). Heinze adds that the ability to set and maintain a navigational bearing is essential for a wide range of navigational applications, including long-range navigation, homing and following a perfectly straight line.

A sweat bee (Megalopta genalis), the species used by Stanley Heinze to delineate his path integration model of navigation.
A sweat bee (Megalopta genalis), the species used by Stanley Heinze to delineate his path integration model of navigation. Photo credit: Ajay Narendra.

Although fruit flies (Drosophila melanogaster) do not have a reputation for migrating, Timothy Warren, Ysabel Giraldo and Michael Dickinson from The California Institute of Technology, USA, suggest that the ubiquitous insects owe their global distribution to an ability to migrate (jeb186148). The flies depend on their knowledge of the position of the sun or moon – gleaned through direct observation, by orientation relative to the pattern of polarized light in the sky, or from the light intensity gradient in the sky – to determine a fixed bearing. Drawing parallels between the structure of the fly central complex and that of the long-distance migratory locust, Warren and colleagues suggest that D. melanogaster select their bearing early in flight, rather than aiming for a genetically preselected goal. They also add that the wealth of molecular tools available to study the minute insects could allow researchers to study the neural circuitry underlying navigation in ways that would be impossible in other species.

A dung beetle rolling a dung ball along a straight line with the bearing shown on a compass.
A dung beetle rolling a dung ball along a straight line with the bearing shown on a compass. Photo credit: Chris Collingridge.

Dung beetles are also not renowned for long-range navigational feats, but Basil el Jundi and a team of international collaborators describe how the insects are able to perform a simpler navigational feat. They roll dung balls in reverse along perfectly straight lines and can even resume their linear path after deviating around bushes and other obstacles. el Jundi explains that the beetles collect a visual snapshot of the sky prior to setting out and process information about the position of the sun, moon or the pattern of polarized light in the sky in the central complex before setting the straight bearing that they follow (jeb192450). Comparing the structure of the dung beetle’s central complex with that of insects that navigate over greater distances, the collaborators admit that they are surprised by the structural similarities despite the vastly different scales of the navigational challenges.

In contrast to the Reviews discussing insect navigation, Francesco Savelli and James Knierim, from Johns Hopkins University, USA, discuss the role of one of the main regions that allows mammals to keep track of their location, the hippocampal formation, which uses landmarks and the sensations generated by the individual’s movements to generate a sense of position (jeb188912). Describing how one class of hippocampus cells, known as ‘place cells’, record the position of an individual in their internal spatial map, the duo discuss ‘grid cells’ – a class of nerve cell that possibly keeps track of an individual’s motion through path integration to generate a sense of position. They go on to review robotic algorithms as well as computer simulations based on the interplay between hippocampal spatial cells, in order to interpret their properties and the function of hippocampal circuits.

Finally, in a second Review discussing the role of grid cells in mammalian navigation, Philippe Gaussier, affiliated with the École Nationale Supérieure de l’Électronique et de ses Applications, France, describes how he and his colleagues use robots that are capable of visual learning and path integration to understand the role of the entorhinal complex – associated with the hippocampus in the mammalian brain – in navigation (jeb186932). However, the team challenges the role of grid cells in the entorhinal complex in path integration, suggesting instead that the structure is a generic merging tool that builds a compact representation of brain activity in other regions implicated in homing and dead-reckoning activities.

Human navigation

How our own navigational skills develop and change as we age has long fascinated psychologists, and Nora Newcombe from Temple University, USA, discusses how infants and children build an understanding of the world around them (jeb186460). Explaining that the development of our ability to navigate is tightly correlated with the emergence of motor skills and our developing senses, Newcombe describes how babies are able to use external cues to learn where objects are located, while toddlers can combine information about other objects in the environment to learn about their surroundings. Although children continue refining their spatial awareness throughout childhood, they may not be able to combine information from our different senses and systems in an optimal way until the ages of 10 or 11, and Newcombe adds that our navigational skills are incomplete until around the age of 12.

Continuing the theme of human navigation, Lucia Jacobs from the University of California, Berkeley, USA, discusses the possibility that following odours for navigation may have driven the development of the distinctive shape of the human nose (jeb186924). Jacobs suggests that competition with other carnivores led Homo sapiens to hunt over long distances in groups before returning with the prey. She explains that this would have necessitated accurate spatial navigation, which could have been made more tractable by the development of stereo olfaction to allow the hunters to locate odours with more precision. However, she adds that since the earliest humans migrated out of Africa there have been many more adaptive pressures on the shape of the nose, accounting for the wide array of shapes that we see today.

In summary

Having compiled this issue dedicated to navigation in collaboration with her colleagues, Webb and el Jundi, Kelber says, ‘I think the collection provides a cross-section of study organisms, the hottest concepts and new methods that will take the field forward’, adding, ‘For anyone interested in the broad topic of animal navigation and its physiological basis, this is better than any textbook. It’s a must-read’. And she is excited about the future. ‘I have two candidates for the next big discovery’, she says: ‘One is unravelling the genetic code for spatial navigation… the other is finding the sensory basis of the magnetic sense that allows animals to find their way’. Whichever wins out first, it is certainly going to be a gripping race.

© 2019. Published by The Company of Biologists Ltd.