Jolyon Troscianko

Image calibration and analysis toolbox – a free software suite for objectively measuring reflectance, colour and pattern

Summary Quantitative measurements of colour, pattern and morphology are vital to a growing range of disciplines. Digital cameras are readily available and already widely used for making these measurements, having numerous advantages over other techniques, such as spectrometry. However, off‐the‐shelf consumer cameras are designed to produce images for human viewing, meaning that their uncalibrated photographs cannot be used for making reliable, quantitative measurements. Many studies still fail to appreciate this, and of those scientists who are aware of such issues, many are hindered by a lack of usable tools for making objective measurements from photographs. We have developed an image processing toolbox that generates images that are linear with respect to radiance from the RAW files of numerous camera brands and can combine image channels from multispectral cameras, including additional ultraviolet photographs. Images are then normalised using one or more grey standards to control for lighting conditions. This enables objective measures of reflectance and colour using a wide range of consumer cameras. Furthermore, if the cameras spectral sensitivities are known, the software can convert images to correspond to the visual system (cone‐catch values) of a wide range of animals, enabling human and non‐human visual systems to be modelled. The toolbox also provides image analysis tools that can extract luminance (lightness), colour and pattern information. Furthermore, all processing is performed on 32‐bit floating point images rather than commonly used 8‐bit images. This increases precision and reduces the likelihood of data loss through rounding error or saturation of pixels, while also facilitating the measurement of objects with shiny or fluorescent properties. All cameras tested using this software were found to demonstrate a linear response within each image and across a range of exposure times. Cone‐catch mapping functions were highly robust, converting images to several animal visual systems and yielding data that agreed closely with spectrometer‐based estimates. Our imaging toolbox is freely available as an addition to the open source ImageJ software. We believe that it will considerably enhance the appropriate use of digital cameras across multiple areas of biology, in particular researchers aiming to quantify animal and plant visual signals.

Extreme binocular vision and a straight bill facilitate tool use in New Caledonian crows.

Humans are expert tool users, who manipulate objects with dextrous hands and precise visual control. Surprisingly, morphological predispositions, or adaptations, for tool use have rarely been examined in non-human animals. New Caledonian crows Corvus moneduloides use their bills to craft complex tools from sticks, leaves and other materials, before inserting them into deadwood or vegetation to extract prey. Here we show that tool use in these birds is facilitated by an unusual visual-field topography and bill shape. Their visual field has substantially greater binocular overlap than that of any other bird species investigated to date, including six non-tool-using corvids. Furthermore, their unusually straight bill enables a stable grip on tools, and raises the tool tip into their visual fields binocular sector. These features enable a degree of tool control that would be impossible in other corvids, despite their comparable cognitive abilities. To our knowledge, this is the first evidence for tool-use-related morphological features outside the hominin lineage.

Tool use by wild New Caledonian crows Corvus moneduloides at natural foraging sites.

New Caledonian crows Corvus moneduloides use tools made from sticks or leaf stems to ‘fish’ woodboring beetle larvae from their burrows in decaying wood. Previous research on this behaviour has been confined to baited sites, leaving its ecological context and significance virtually unexplored. To obtain detailed observations of natural, undisturbed tool use, we deployed motion-triggered video cameras at seven larva-fishing sites. From 1797 camera hours of surveillance over 111 days, we recorded 317 site visits by at least 14 individual crows. Tool use was observed during 150 site visits. Our video footage revealed notable variation in foraging success among identifiable crows. Two nutritionally independent, immature crows spent considerable time using tools, but were much less successful than local adults, highlighting the potential role of individual and social learning in the acquisition of tool-use proficiency. During systematic surveys of larva-fishing sites, we collected 193 tools that crows had left inserted in larva burrows. Comparing these tools with the holes in which they were found, and with raw materials available around logs, provides evidence for tool selectivity by New Caledonian crows under natural conditions. Taken together, these two complementary lines of investigation provide, to our knowledge, the first quantitative description of larva fishing by wild crows in its full ecological context.

Repeated targeting of the same hosts by a brood parasite compromises host egg rejection

Cuckoo eggs famously mimic those of their foster parents to evade rejection from discriminating hosts. Here we test whether parasites benefit by repeatedly parasitizing the same host nest. This should make accurate rejection decisions harder, regardless of the mechanism that hosts use to identify foreign eggs. Here we find strong support for this prediction in the African tawny-flanked prinia (Prinia subflava), the most common host of the cuckoo finch (Anomalospiza imberbis). We show experimentally that hosts reject eggs that differ from an internal template, but crucially, as the proportion of foreign eggs increases, hosts are less likely to reject them and require greater differences in appearance to do so. Repeated parasitism by the same cuckoo finch female is common in host nests and likely to be an adaptation to increase the probability of host acceptance. Thus, repeated parasitism interacts with egg mimicry to exploit cognitive and sensory limitations in host defences.

An EST screen from the annelid Pomatoceros lamarckii reveals patterns of gene loss and gain in animals

BackgroundSince the drastic reorganisation of the phylogeny of the animal kingdom into three major clades of bilaterians; Ecdysozoa, Lophotrochozoa and Deuterostomia, it became glaringly obvious that the selection of model systems with extensive molecular resources was heavily biased towards only two of these three clades, namely the Ecdysozoa and Deuterostomia. Increasing efforts have been put towards redressing this imbalance in recent years, and one of the principal phyla in the vanguard of this endeavour is the Annelida.ResultsIn the context of this effort we here report our characterisation of an Expressed Sequence Tag (EST) screen in the serpulid annelid, Pomatoceros lamarckii. We have sequenced over 5,000 ESTs which consolidate into over 2,000 sequences (clusters and singletons). These sequences are used to build phylogenetic trees to estimate relative branch lengths amongst different taxa and, by comparison to genomic data from other animals, patterns of gene retention and loss are deduced.ConclusionThe molecular phylogenetic trees including the P. lamarckii sequences extend early observations that polychaetes tend to have relatively short branches in such trees, and hence are useful taxa with which to reconstruct gene family evolution. Also, with the availability of lophotrochozoan data such as that of P. lamarckii, it is now possible to make much more accurate reconstructions of the gene complement of the ancestor of the bilaterians than was previously possible from comparisons of ecdysozoan and deuterostome genomes to non-bilaterian outgroups. It is clear that the traditional molecular model systems for protostomes (e.g. Drosophila melanogaster and Caenorhabditis elegans), which are restricted to the Ecdysozoa, have undergone extensive gene loss during evolution. These ecdysozoan systems, in terms of gene content, are thus more derived from the bilaterian ancestral condition than lophotrochozoan systems like the polychaetes, and thus cannot be used as good, general representatives of protostome genomes. Currently sequenced insect and nematode genomes are less suitable models for deducing bilaterian ancestral states than lophotrochozoan genomes, despite the array of powerful genetic and mechanistic manipulation techniques in these ecdysozoans. A distinct category of genes that includes those present in non-bilaterians and lophotrochozoans, but which are absent from ecdysozoans and deuterostomes, highlights the need for further lophotrochozoan data to gain a more complete understanding of the gene complement of the bilaterian ancestor.

Camouflage predicts survival in ground-nesting birds

Evading detection by predators is crucial for survival. Camouflage is therefore a widespread adaptation, but despite substantial research effort our understanding of different camouflage strategies has relied predominantly on artificial systems and on experiments disregarding how camouflage is perceived by predators. Here we show for the first time in a natural system, that survival probability of wild animals is directly related to their level of camouflage as perceived by the visual systems of their main predators. Ground-nesting plovers and coursers flee as threats approach, and their clutches were more likely to survive when their egg contrast matched their surrounds. In nightjars – which remain motionless as threats approach – clutch survival depended on plumage pattern matching between the incubating bird and its surrounds. Our findings highlight the importance of pattern and luminance based camouflage properties, and the effectiveness of modern techniques in capturing the adaptive properties of visual phenotypes.

Defeating crypsis: detection and learning of camouflage strategies.

Camouflage is perhaps the most widespread defence against predators in nature and an active area of interdisciplinary research. Recent work has aimed to understand what camouflage types exist (e.g. background matching, disruptive, and distractive patterns) and their effectiveness. However, work has almost exclusively focused on the efficacy of these strategies in preventing initial detection, despite the fact that predators often encounter the same prey phenotype repeatedly, affording them opportunities to learn to find those prey more effectively. The overall value of a camouflage strategy may, therefore, reflect both its ability to prevent detection by predators and resist predator learning. We conducted four experiments with humans searching for hidden targets of different camouflage types (disruptive, distractive, and background matching of various contrast levels) over a series of touch screen trials. As with previous work, disruptive coloration was the most successful method of concealment overall, especially with relatively high contrast patterns, whereas potentially distractive markings were either neutral or costly. However, high contrast patterns incurred faster decreases in detection times over trials compared to other stimuli. In addition, potentially distractive markings were sometimes learnt more slowly than background matching markings, despite being found more readily overall. Finally, learning effects were highly dependent upon the experimental paradigm, including the number of prey types seen and whether subjects encountered targets simultaneously or sequentially. Our results show that the survival advantage of camouflage strategies reflects both their ability to avoid initial detection (sensory mechanisms) and predator learning (perceptual mechanisms).

Motion dazzle and the effects of target patterning on capture success

BackgroundStripes and other high contrast patterns found on animals have been hypothesised to cause “motion dazzle”, a type of defensive coloration that operates when in motion, causing predators to misjudge the speed and direction of object movement. Several recent studies have found some support for this idea, but little is currently understood about the mechanisms underlying this effect. Using humans as model `predators’ in a touch screen experiment we investigated further the effectiveness of striped targets in preventing capture, and considered how stripes compare to other types of patterning in order to understand what aspects of target patterning are important in making a target difficult to capture.ResultsWe find that striped targets are among the most difficult to capture, but that other patterning types are also highly effective at preventing capture in this task. Several target types, including background sampled targets and targets with a ‘spot’ on were significantly easier to capture than striped targets. We also show differences in capture attempt rates between different target types, but we find no differences in learning rates between target types.ConclusionsWe conclude that striped targets are effective in preventing capture, but are not uniquely difficult to catch, with luminance matched grey targets also showing a similar capture rate. We show that key factors in making capture easier are a lack of average background luminance matching and having trackable ‘features’ on the target body. We also find that striped patterns are attempted relatively quickly, despite being difficult to catch. We discuss these findings in relation to the motion dazzle hypothesis and how capture rates may be affected more generally by pattern type.

Color contrast and stability as key elements for effective warning signals

Vivid warning signals (aposematism) have evolved repeatedly throughout the animal kingdom. However, relatively few studies consider what makes an effective signal, such as in terms of preventing attack and promoting avoidance learning by predators. Signal form varies substantially among and sometimes within species, but there has also been apparent convergence on relatively few main color types. We aimed to determine why warning signals often combine red, orange, yellow and black colors, and specifically to determine whether these colors provide highly salient and reliable visual signals under a range of environmental conditions. Using digital image analysis, we modeled ladybird (ladybug) coloration to an avian visual system. We calculated the contrast of several different ladybird species against an average green background, based on predicted opponent color channel responses in bird vision. Our results suggest that longwave colors (i.e. red, orange) are more contrasting than colors such as blue, against green natural backgrounds. Moreover, these colors yield relatively unchanging (stable) signals throughout the day and under different weather conditions. These analyses show how aposematic signals have evolved under selection to be more effective by being more conspicuous and reliable to the visual system of their potential avian predators.

Changes in women’s facial skin color over the ovulatory cycle are not detectable by the human visual system

Human ovulation is not advertised, as it is in several primate species, by conspicuous sexual swellings. However, there is increasing evidence that the attractiveness of women’s body odor, voice, and facial appearance peak during the fertile phase of their ovulatory cycle. Cycle effects on facial attractiveness may be underpinned by changes in facial skin color, but it is not clear if skin color varies cyclically in humans or if any changes are detectable. To test these questions we photographed women daily for at least one cycle. Changes in facial skin redness and luminance were then quantified by mapping the digital images to human long, medium, and shortwave visual receptors. We find cyclic variation in skin redness, but not luminance. Redness decreases rapidly after menstrual onset, increases in the days before ovulation, and remains high through the luteal phase. However, we also show that this variation is unlikely to be detectable by the human visual system. We conclude that changes in skin color are not responsible for the effects of the ovulatory cycle on women’s attractiveness.