Ants Use Multiple Spatial Memories and Chemical Pointers to Navigate Their Nest

摘要

class="head no_bottom_margin" id="sec1title">IntroductionNavigation is a major component in the adaptive and ecological success of any animal species. Different environments demand different navigational strategies as they vary in their resource distribution, the sensory cues they offer, and their topological structure. The vast majority of current knowledge concerns navigation above ground, which heavily relies on visual cues and often takes place in environments, either two- or three-dimensional, that allow for relatively unconstrained motion. Life, however, also inhabits subterranean environments. Navigation in these dark constrained conditions (, , ) is far less understood.Ants have attracted special attention in the study of navigation. Different ant species exhibit exceptional navigational skills despite an extremely small brain size (, ). This has allowed for an extensive study of ant navigational strategies, of the mechanisms that underlie ant navigation, and of its ecological costs and benefits (, , , , ). Similar to other species, ants depend on visual cues for navigation to a great extent (), even when walking along pheromone trails (, ) or during nocturnal activity (, ). Correspondingly, the vast majority of research on ant navigation concerns movement on the surface of the ground. This stands at odds with the fact that ants spend a considerable fraction of their lives within their nests (href="#bib24" rid="bib24" class=" bibr popnode">Heyman et al., 2017).The navigational capabilities that ants display above ground do not stop at the nest entrance: ants have preferred locations within the nest (href="#bib48" rid="bib48" class=" bibr popnode">Sendova-Franks and Franks, 1995, href="#bib39" rid="bib39" class=" bibr popnode">Mersch et al., 2013) to which they return repeatedly (href="#bib24" rid="bib24" class=" bibr popnode">Heyman et al., 2017). However, many of the navigation strategies that ants employ above the ground cannot be expected to carry over to intranidal navigation. Light does not penetrate underground. This renders the prevalent strategies of visual beaconing (href="#bib64" rid="bib64" class=" bibr popnode">Wehner et al., 1996, href="#bib20" rid="bib20" class=" bibr popnode">Graham et al., 2003, href="#bib34" rid="bib34" class=" bibr popnode">McLeman et al., 2002) and image matching (href="#bib30" rid="bib30" class=" bibr popnode">Lent et al., 2010) useless. Moreover, celestial bodies, often used as global positioning cues in various navigation mechanisms, are inaccessible. Here, we study the cues that are available underground and the ways in which ants integrate them into their navigational decisions.What sources of navigational information are accessible inside the ant nest? Gravitational signals may account for an ant colony's organization along the vertical axis (href="#bib56" rid="bib56" class=" bibr popnode">Tschinkel, 1999, href="#bib57" rid="bib57" class=" bibr popnode">Tschinkel, 2003, href="#bib55" rid="bib55" class=" bibr popnode">Tschinkel, 2005, href="#bib58" rid="bib58" class=" bibr popnode">Tschinkel and Hanley, 2017), whereas magnetic sensation (href="#bib1" rid="bib1" class=" bibr popnode">Anderson and Vander Meer, 1993) could play a similar role in the horizontal direction. Chemical-encoded information is another possible source of navigational cues within the nest. Above ground such cues come in the form of pheromone trails (href="#bib70" rid="bib70" class=" bibr popnode">Holldobler and Wilson, 1990, href="#bib12" rid="bib12" class=" bibr popnode">David Morgan, 2009, href="#bib11" rid="bib11" class=" bibr popnode">Czaczkes et al., 2015), hydrocarbon gradients (href="#bib52" rid="bib52" class=" bibr popnode">Sturgis et al., 2011), and volatile chemical gradients (href="#bib51" rid="bib51" class=" bibr popnode">Steck et al., 2011, href="#bib3" rid="bib3" class=" bibr popnode">Buehlmann et al., 2012). The role of CO2 soil gradients in colony organization was studied within natural nests (href="#bib59" rid="bib59" class=" bibr popnode">Tschinkel, 2013). Recently, it was shown that chemical navigational cues within the nest allow the ants to distinguish between different nest chambers (href="#bib24" rid="bib24" class=" bibr popnode">Heyman et al., 2017).Spatial memory may also be useful within the dark confines of the nest. An appealing mechanism in this respect is path integration, a prevalent navigational strategy that was studied mostly above ground but could potentially remain efficient under it (href="#bib27" rid="bib27" class=" bibr popnode">Kimchi et al., 2004) because ants were shown to perform path integration, which includes vertical components (href="#bib67" rid="bib67" class=" bibr popnode">Wohlgemuth et al., 2001). Another possible mechanism is motor learning, wherein movement sequences are memorized (href="#bib50" rid="bib50" class=" bibr popnode">Stamps, 1995, href="#bib49" rid="bib49" class=" bibr popnode">Srinivasan and Zhang, 2004). Ants were shown to apply motor learning while navigating in mazes with no visual landmarks (href="#bib33" rid="bib33" class=" bibr popnode">Macquart et al., 2008). Such self-referenced mechanisms reduce the dependence on external reference points, which may be unavailable within the nest (href="#bib6" rid="bib6" class=" bibr popnode">Collett and Collett, 2000, href="#bib62" rid="bib62" class=" bibr popnode">Wehner, 2003, href="#bib26" rid="bib26" class=" bibr popnode">Jeffery, 2003). However, independence from external references has its limitations: path integration must be accompanied by other navigational mechanisms to avoid runaway errors (href="#bib36" rid="bib36" class=" bibr popnode">Merkle et al., 2006, href="#bib38" rid="bib38" class=" bibr popnode">Merkle and Wehner, 2009, href="#bib41" rid="bib41" class=" bibr popnode">Müller and Wehner, 1988), whereas motor learning requires practicing the same route many times (href="#bib50" rid="bib50" class=" bibr popnode">Stamps, 1995).Ants combine private and social cues in a variety of contexts (href="#bib7" rid="bib7" class=" bibr popnode">Cronin, 2013, href="#bib46" rid="bib46" class=" bibr popnode">Robinson et al., 2009, href="#bib10" rid="bib10" class=" bibr popnode">Czaczkes et al., 2011). Social information, which is formed by the combined knowledge of many individuals, is often reliable and stable (href="#bib17" rid="bib17" class=" bibr popnode">Galton, 1907) yet slow to respond to environmental changes (href="#bib15" rid="bib15" class=" bibr popnode">Feldman et al., 1996). In contrast, private information, which is based on individual learning, has shorter update times but is error-prone (href="#bib36" rid="bib36" class=" bibr popnode">Merkle et al., 2006, href="#bib38" rid="bib38" class=" bibr popnode">Merkle and Wehner, 2009, href="#bib41" rid="bib41" class=" bibr popnode">Müller and Wehner, 1988). The latter source of information becomes crucial in situations of rapid environmental changes where social information is either missing or misleading (href="#bib23" rid="bib23" class=" bibr popnode">Harrison et al., 1989). These two information sources therefore complement one another to allow for organized and adaptive behaviors (href="#bib45" rid="bib45" class=" bibr popnode">Rieucau and Giraldeau, 2011, href="#bib53" rid="bib53" class=" bibr popnode">Templeton and Giraldeau, 1995).In this article, we use the brood-retrieval behavior of the species Camponotus fellah, to study how ants navigate their nest. We do this by tracking the trajectories of ants as they move from a misplaced brood pile outside the nest to a target chamber within the nest. We analyze which cues play important roles in the different parts of this trajectory. We find that, to navigate within the nest, the ants combine three independent sources of information. First are self-referenced cues where the ants memorize multiple target locations and orient toward them with no requirement for any visual or olfactory cues. Second are socially generated chemical cues that are placed at decision points located away from the destination and mark the route toward it. Third, we show that ant navigation is assisted by global gravitational cues. We go on to show how ants combine these different information sources and how individuals can adjust the weight attributed to conflicting cues in a way that allows them to adopt new routes while abandoning unrewarding ones. This fast individual learning process leads to global, stable improvement in the collective performance of the colony.