Detection experiments with humans implicate visual predation as a driver of colour polymorphism dynamics in pygmy grasshoppers

Abstract

Background: Animal colour patterns offer good model systems for studies of biodiversity and evolution of local adaptations. An increasingly popular approach to study the role of selection for camouflage for evolutionary trajectories of animal colour patterns is to present images of prey on paper or computer screens to human 'predators'. Yet, few attempts have been made to confirm that rates of detection by humans can predict patterns of selection and evolutionary modifications of prey colour patterns in nature. In this study, we first analyzed encounters between human 'predators' and images of natural black, grey and striped colour morphs of the polymorphic Tetrix subulata pygmy grasshoppers presented on background images of unburnt, intermediate or completely burnt natural habitats. Next, we compared detection rates with estimates of capture probabilities and survival of free-ranging grasshoppers, and with estimates of relative morph frequencies in natural populations.

Results: The proportion of grasshoppers that were detected and time to detection depended on both the colour pattern of the prey and on the type of visual background. Grasshoppers were detected more often and faster on unburnt backgrounds than on 50% and 100% burnt backgrounds. Striped prey were detected less often than grey or black prey on unburnt backgrounds; grey prey were detected more often than black or striped prey on 50% burnt backgrounds; and black prey were detected less often than grey prey on 100% burnt backgrounds. Rates of detection mirrored previously reported rates of capture by humans of free-ranging grasshoppers, as well as morph specific survival in the wild. Rates of detection were also correlated with frequencies of striped, black and grey morphs in samples of T. subulata from natural populations that occupied the three habitat types used for the detection experiment.

Conclusions: Our findings demonstrate that crypsis is background-dependent, and implicate visual predation as an important driver of evolutionary modifications of colour polymorphism in pygmy grasshoppers. Our study provides the clearest evidence to date that using humans as 'predators' in detection experiments may provide reliable information on the protective values of prey colour patterns and of natural selection and microevolution of camouflage in the wild.

Figure 1

Increase in number of published studies that have used humans as ‘predators’ in detection experiments investigating various aspects of protective coloration. Figure shows cumulative number of studies. For list of references, see Additional file 1.

Figure 2

Images of prey colour morphs and visual backgrounds used in detection experiment.Tetrix subulata pygmy grasshoppers representing black, grey and striped colour morphs (a). Images of T. subulata presented on photographic samples of natural backgrounds from non-burnt environment (b), and from post-fire environments representing 50% burnt substrate (c), and 100% burnt substrate (d). White circles denote the location of the grasshoppers. In the experiment only one grasshopper at the time was presented however in order to illustrate the differences between the colour morph on each background we present all of them in one image. Photo: E. Karpestam.

Figure 3

Results from detection experiment. Estimated rates of detection by human ‘predators’ of images of black (black circles), grey (open circles) and striped (grey circles) Tetrix subulata pygmy grasshoppers presented on a computer screen against images of natural unburned greenish (0% burnt), intermediate (50% burnt) and totally burned (100% burnt) visual backgrounds. Average percent detected grasshopper images (a). Average time to detection based on data for only those images that were detected (b). Figure shows mean ± s.e. Means with different letters are significantly different, as revealed by Student-Newman-Keuls a posteriori pair-wise comparisons of colour morph group means within each background.

Figure 4

Comparisons between detection rate, capture probability and survival in the wild. Relationship between rate of detection by humans of images of three pygmy grasshopper colour morphs (striped, black and grey) presented against samples of visual backgrounds on a computer screen and rate of capture (a) and rate of survival (b) of free-ranging female (open symbols) and male (black symbols) live grasshoppers in the wild. Estimates of capture and total survival rate in the wild were computed from mark-recapture data. Total survival rate was computed as the product of survival probabilities for 5 separate time periods for each morph and sex. For details see Forsman and Appelqvist [29]. Figure shows mean ± s.e.

Figure 5

Association between detection rates and morph frequencies in natural populations. Relative frequencies of three pygmy grasshopper colour morphs (striped, black and grey) in natural populations from three habitat types (100% burned, 50% burned and unburnt) are negatively correlated (r_s = −0.71, n = 9, p = 0.032) with rates of detection by humans of images of grasshopper colour morphs presented against samples of visual backgrounds on a computer screen. Relative morph frequencies in the wild were estimated from data for 4,091 individuals comprising 6 samples from recently burnt (1 year after fire) habitats, 7 samples from populations in areas that had burnt 3 or 4 years prior to collection, and 14 samples from populations in unburnt areas (see Table 1). Figure shows means. Dotted and dashed lines indicate relationships among morphs within each of the three backgrounds, and the thick line indicates relationship among morphs across all backgrounds.