Search image formation for spider prey in a mud dauber wasp.

Highlights

• Mud dauber wasps capture spiders, paralyse and then oviposit on them in sequentially built cells.

• Traits used by the wasp, such as spider colour and pattern, can be quantified.

• Change in traits across time can be measured.

• Wasps show preference for certain colours and patterns which remains constant across time.

• This suggests that wasps use a search image strategy in predation.

Abstract

Search images are perceptual biases acquired through experience that improve an individual’s ability to detect the object of their search (e.g., a predator seeking prey). In hymenopterans, examples include floral search images in bees and acquired sensory biases towards specific prey in wasp predators. Mud dauber wasps exhibit individual specialization and consistency in prey preferences through time, often based on visual and chemical cues, that may vary at intraspecific levels. However, the search image concept in wasps has not been evaluated from a visual ecology perspective. Using psychophysical visual modelling from multispectral digital photography, we measured the colour and body pattern of the spiders captured and stored in nests by the wasp Trypoxylon mexicanum. Those visual traits were compared at the community and nest cell levels, according to the nest provisioning sequence, and its relationship with spider diversity. Our results show that the wasps are choosing a small group of orb weavers (Araneidae) with similar coloration and body patterns. These findings highlight the specific visual features that may be the focal trait during search image formation in these wasps. The colour and pattern variables of spider prey were consistent over time, suggesting that individual search images may strengthen with experience.

Introduction

Navigating through a world full of multi-sensory stimuli is a challenge for predators. They receive, discriminate, and decide based on different inputs perceived by their sensory systems, which are the biological interface between the environment and the organism (Barth and Schmid, 2001). Whether detecting potential prey, escaping from a predator, or monitoring the surroundings, animal senses are optimized to meet their ecological needs (Stevens, 2013). While foraging, predators use memory, perception, timing, and spatial ability to ensure a successful hunt (Stephens et al., 2008).

Cognition plays an essential role in animal foraging behaviour (Adams-Hunt and Jacobs, 2008). One of the cognitive phenomena involved in this task is search image formation, which consists of perceptual biases that improve the predator’s ability to detect a particular prey as a result of past encounters with that prey type (Tinbergen, 1960). Search images are thought to arise due to the benefits in reducing the cognitive load associated with processing complex information or by increasing selective attention to cues associated with particular prey types (Dukas and Kamil, 2001).

The concept of image formation was initially applied to predators foraging for cryptic prey (see Dukas and Ellner, 1993; Dukas, 2002; Langley, 1996). However, it has been suggested that ‘visually salient’ conspicuous targets also favour forming a search image in the predator learning process (Itti and Koch, 2001). This may be due to the relationship of search image formation process with selective attention, which is a consequence of constraints of cognition and may favour constancy in target selection (Goulson, 2000).

In terms of visual signalling, floral constancy in hymenopteran insects (i.e., when pollinators tend to restrict their visits to only a few of the available plant species; Chittka et al., 1999), could be the result of search image formation. Goulson (2000) suggested that hymenopterans foraging for flowers have a limited ability to process visual information from many floral displays simultaneously and so selectively attend to certain features of their preferred flowers (but see Gegear and Laverty, 2001 for further discussion). Hymenopterans are known to compensate for illumination changes (i.e., colour constancy) in identifying natural colours and patterns under different light conditions and thus recognize a preferred flower efficiently (Foster, 2011).

Parasitic wasps are a promising model for studying the role of learning and search images in modulating behavioural decisions. A good example is the foraging behaviour of araneophagic mud dauber wasps (Crabronidae and Sphecidae; Cloudsley-Thompson, 1995). These wasps also have individual variation in prey preference in a population, resulting from learning search images (visual, olfactory, or both) formed/reinforced on early foraging flights (Powell and Taylor, 2017). Thus, individual wasps form strong preferences for a specific subset of the available spider species, such as web builders (Araújo and Gonzaga, 2007, Pitilin et al., 2012) or ambusher-stalkers (Musicante and Salvo, 2010).

The response to prey traits, probably modified by foraging experience, could improve subsequent foraging efficiency on available hosts, resulting in search image formation that may shape dietary breadth (Ishii and Shimada, 2009, shii and Shimada, 2012). Prey detection and recognition in mud dauber wasps involves chemical and visual cues (Uma et al., 2013, Uma and Weiss, 2010) and conspicuous spiders are more likely to be captured (Robledo-Ospina et al., 2021). However, spiders have a high diversity of body colouration and patterns that vary both inter-and intra-specifically (Hsiung et al., 2019, Oxford and Gillespie, 1998). Hence, the evaluation of body pattern colouration through time during nest provisioning could better inform the role these traits might play in the foraging strategies and search image formation of individual wasps.

By collecting mud dauber wasp nests in natural conditions, it is possible to have a complete catalogue of different prey traits chosen by the female (e.g., sex, developmental stage, size, and body colouration) even without observing prey capture directly (Muma and Jeffers, 1945, Patil and Arade, 2011, Robledo-Ospina et al., 2021). Consequently, applying the search image formation concept in a broad sense and considering the natural diversity of spider colouration, we aimed to evaluate the variation of spider body colouration and patterns using psychophysical colour spaces as a function of the prey diversity and time during the nest construction sequence in nests of Trypoxylon (Trypargilum) mexicanum Saussure, 1867 (Hymenoptera: Crabronidae). We predicted that if spider body colouration and patterns play an essential role in the wasp’s search image formation process, we would observe low or decreasing variation in colour diversity and pattern diversity over time. Furthermore, we expected that spiders selected by individual wasps should exhibit high visual similarity as perceived through the wasp visual system.