Egg discrimination along a gradient of natural variation in eggshell coloration

Abstract

Accurate recognition of salient cues is critical for adaptive responses, but the underlying sensory and cognitive processes are often poorly understood. For example, hosts of avian brood parasites have long been assumed to reject foreign eggs from their nests based on the total degree of dissimilarity in colour to their own eggs, regardless of the foreign eggs' colours. We tested hosts' responses to gradients of natural (blue-green to brown) and artificial (green to purple) egg colours, and demonstrate that hosts base rejection decisions on both the direction and degree of colour dissimilarity along the natural, but not artificial, gradient of egg colours. Hosts rejected brown eggs and accepted blue-green eggs along the natural egg colour gradient, irrespective of the total perceived dissimilarity from their own egg's colour. By contrast, their responses did not vary along the artificial colour gradient. Our results demonstrate that egg recognition is specifically tuned to the natural gradient of avian eggshell colour and suggest a novel decision rule. These results highlight the importance of considering sensory reception and decision rules when studying perception, and illustrate that our understanding of recognition processes benefits from examining natural variation in phenotypes.

Keywords: brood parasitism; colour perception; decision-making; egg discrimination; recognition.

Figure 1.

Decision-making by hosts of avian brood parasites is an ideal system for studying general principles of cognition in nature. These hosts must detect and appropriately respond to a brood parasite's trickery while balancing the risk of acceptance or rejection errors (striped and cross-hatched areas, respectively). The acceptance threshold (dashed vertical lines) lies at the intersection of these risks [14], such that stimuli between both thresholds are accepted and beyond which stimuli are rejected. These thresholds can shift (infinitely far) depending on perceived risk (bi-directional arrows on acceptance thresholds), making them akin to decision boundaries in general recognition theory [15] rather than demarcating a host's perceptual limits (i.e. psychological versus psychophysical). In the top portion of each schematic (a,b) we illustrate a distribution of host eggshell phenotypes (middle) and distributions for two parasites (left and right). The traditional expectation based on multiple thresholds (a, bottom) is that as the magnitude of perceived difference between host and parasitic eggs increases hosts are more likely to respond; therefore, blue-green and brown parasitic eggs that are equally different to the host's eggs should be rejected at equal rates. However, if hosts base rejection decisions on (b) specific colours, then we expect (b, bottom) that rejections would be biased toward one end of the phenotypic range, despite the absolute perceived difference; for example, such that either blue-green or brown parasitic eggs are rejected.

Figure 2.

Foreign eggs were (a) painted across two gradients of variation that either align (blue-green to brown) or are orthogonal (green to purple) with natural eggshell colours. These manipulations produced perceivable colour variation that represents relevant threats and novel stimuli to hosts (see the electronic supplementary material). These models, presented to (b) blackbirds and (c) robins, were specifically designed with respect to the avian tetrahedral colour space (shown from above). Within each tetrahedron we illustrate the predicted short ‘S’, medium ‘M’, long ‘L’, and ultraviolet ‘U’ wavelength-sensitive photoreceptor stimulation when these foreign eggs are viewed by the host. Insets show these models (in actual colour) alongside variation of natural (b) blackbird and (c) robin eggshell colours (black dots within each inset). For the purpose of comparison, we show eggshell coloration of the brown-headed cowbird (red dots in c) that parasitizes the robin (data from [16]).

Figure 3.

The probability of rejecting a coloured foreign egg is shown for (a,b) blackbirds (n = 82) and (c,d) robins (n = 52), with respect to the position of each hosts' own egg colour (see inset eggs above zero on both x-axes) along the (a,c) blue-green to brown and (b,d) purple to green colour gradients (in JNDs). We show a significant logistic (solid line, table 1), Gaussian (dashed, electronic supplementary material, table S2), and Weibull (dotted, electronic supplementary material, table S3) fits. Please note, we plotted all egg rejections, including rejection errors (black dots; n = 2) and foreign eggs falling along both colour dimensions. For comparison, we plotted (c) the mean location (approx. 4 JND on the x-axis) of eggshell coloration along this axis for the robin's heterospecific brood parasite, the brown-headed cowbird (also see figure 2). We illustrate 10 000 resampled slopes from binomial models predicting host behavioural responses (light grey lines); refer to table 1 for the significance of these parameters.