We show here that the wood ants’ innate visual attraction is not context-dependent, but an intrinsic visuomotor response seen across different motivational and ecological scenarios. More specifically, foragers with different motivational states, i.e., unfed or fed, as well as males that show no foraging behavior naturally, all show an innate visual attraction to conspicuous visual objects (Fig. 1).
Conspicuous objects initiate intrinsic visuomotor response
Many insects show intrinsic visuomotor response, i.e., they show fixed motor behaviors in response to specific visual input. Wood ant foragers show an innate attraction to large and conspicuous objects (Buehlmann et al. 2020a, c; Graham et al. 2003; Voss 1967), whereas foragers from other ant species with different foraging ecologies show innate attractions different to wood ants (e.g., (Collett 2010; Heusser and Wehner 2002)). Wood ants inhabit cluttered woodland habitat and feed predominantly on honeydew from aphids on trees (Domisch et al. 2016), hence, the attraction to ‘tree-like’ objects might be an ecologically relevant behavior that is tailored to the wood ants’ foraging ecology (Graham and Wystrach 2016).
Ants that rely on vision predominantly for navigation do not have a high visual resolution, but the ants’ wide-field and low-resolution vision allows robust visual navigation using the visual information provided by the environment. We do not know the exact details of the wood ants’ visual system, but the Australian desert ant that is a visual navigator in a similarly cluttered habitat has a horizontal visual field of approximately 150° per eye and an interommatidial angle of 3.7° (Schwarz et al. 2011). Which means that large conspicuous objects, such as tree trunks, would be easily perceivable (Supplementary Fig. 1).
What is the role of innate behaviors in navigation?
We show here that innate visual orientation in wood ants is not controlled by the ants’ food-related motivational state, however, innate behaviors still play an important role during navigation for foraging. Path integration (e.g., (Collett et al. 2001; Mueller and Wehner 2010)), pheromone trails (e.g., (Harrison et al. 1989)), or innately attractive visual cues (e.g., (Collett 2010; Graham et al. 2003)) are innate strategies that are important for naive foragers or experienced ants exploring unfamiliar environments. As with path integration or odor trails, innate visual responses are intrinsic visuomotor responses that act as a scaffold by structuring the ants’ paths and thus facilitate the learning of sensory cues that are necessary for successful navigation (Graham et al. 2003). More specifically, incorporating these innate visual responses in route learning allows ants to take the same path repeatedly. Ants will thereby experience consistent views which accelerates the acquisition of visual information along the route. Additionally, it increases the robustness of learnt visual routes (Graham et al. 2003). Taken together, innate and learnt navigational strategies interact and allow the ants to successfully navigate between their nest and feeding sites (Buehlmann et al. 2020b; Knaden and Graham 2016). In male ants, it is possible that they are attracted to conspicuous objects to gain elevation to assist in dispersal. However, any role in innate visual orientation that assists in foraging would expect to be modulated by the ants’ motivational state (i.e., fed vs unfed foragers).
Experienced ant foragers navigate along routes using learnt visual information (Graham and Philippides 2017; Wehner et al. 2014; Zeil 2012). In a set of experiments, ant foragers were trained to learn visual cues along a route to a feeder and well-trained ants were subsequently tested with different motivational states (Harris et al. 2005; Wehner et al. 2006). Different behaviors were recorded in fed and unfed ant foragers, i.e., the ants’ motivational state played an important role in organizing visual navigational memories in ants navigating along learnt routes (Harris et al. 2005; Wehner et al. 2006). Hence, different to what we have shown here for innate visual responses, visual route memories are primed by the ants’ feeding state and this controls the choice between foodward and homeward route memories (Harris et al. 2005).
Is it a surprise that innate visual responses are not flexible?
There are several examples of flexible innate behaviors in insects that can be modulated by the animals’ feeding state. For example, it was shown in parasitoid wasps that the insects’ individual feeding state controls their innate behavior (Waeckers 1994). Unfed wasps are attracted by flower odors and yellow targets that indicate food while fed wasps are attracted to host odors and are not attracted by yellow colors (Waeckers 1994). Other experiments have shown that the visual saliency can be modulated by the presence of odors. For instance, experiments in fruit flies have revealed that appetitive odors enhance the flies’ approach to visual cues (Cheng and Frye 2021). Furthermore, experiments with hawkmoths have shown that the moths’ innate color preference depends on ambient light conditions (Kuenzinger et al. 2019). These moths are crepuscular, and their color preferences are tuned to illuminance and background. This flexible behavior allows them to successfully forage under different light conditions. These examples show that insects are equipped with innate visual preferences, but in some species necessary behavioral flexibility is maintained and behaviors are tuned to foraging ecology.
Given that there are many examples of flexibility, there is the question as to why wood ants do not show any flexibility in their innate visual orientation to conspicuous objects. One reason could be that ant foragers rely on their multimodal navigation toolkit which overcomes potential problems with an inflexible innate visual reflex. Fed foragers will have path integration information and learnt odor cues and visual information (Buehlmann et al. 2020b) as they attempt to return to their nest and these sources of orientation information may be more than enough to overcome innate visual attractions (Buehlmann et al. 2020c; Harris et al. 2007; Schwarz and Cheng 2010) that may otherwise disrupt a homeward journey.
Innate visual attraction in the insect brain
Recent research on the central complex (CX), a brain area located at the midline of the insect brain, revealed its importance in navigational tasks (Fisher 2022). Work on ring neurons in the central complex of the fruit fly showed that many of these neurons preferentially respond to vertically oriented objects (Seelig and Jayaraman 2013) and computational simulations further revealed that the sparse encoding in a population of these visually responsive ring neurons is sufficient to explain the innate behavior observed in flies (Dewar et al. 2017; Wystrach et al. 2014). More specifically, the activity of these neurons was highest when the agent was facing a narrow vertical bar or an inner edge of a wide vertical bar. Furthermore, when exposed to natural scenes, these cells preferentially respond when facing large high contrast objects such as trees (Dewar et al. 2017; Wystrach et al. 2014). Finally, as previously mentioned, innate visual responses are intrinsic visuomotor responses that act as a scaffold by structuring paths and thus facilitate the learning of sensory cues that are necessary for navigation along a route (Graham et al. 2003). During this learning, innate behaviors are over-ridden but not changed, hence, the insect keeps the innate responses as a backup (Goulard et al. 2021). It thus makes sense that the ants’ motivational state controls visual memory along a learnt route (Harris et al. 2005; Wehner et al. 2006), but that there is no flexibility in intrinsic visuomotor responses (Fig. 1).