Author: Danielle Klomp

The use of programmable robots (‘mechanical models’ is more accurate) to minimise disturbance while observing wildlife, or to run behavioural experiments in the field, has slowly increased in the last decade and studies across many taxa have utilized this approach (Martins et al., 2005; Partan et al., 2009; Cianca et al., 2013; Macedonia et al., 2013; Clark et al., 2015). I’d argue that “robots” are one for the most important tools for behavioural ecologists studying communication or display behaviour, as they are one of the few ways in which we can conduct field-based experiments – mimicking or manipulating animal behaviour, colour or morphology in any way – in the animal’s natural environment.

We recently published a paper in the Journal of Evolutionary Biology, using robots in playback experiments to test the importance of ornament design for signal detection and conspecific recognition.

Many factors potentially affect signal design, including the need for rapid signal detection and the ability to identify the signal as conspecific. As understanding these different sources of selection on signal design is essential in the larger goal of explaining the evolution of both signal complexity and signal diversity, here we assessed the relative importance of detection and recognition for signal design in the Black-bearded gliding lizard, Draco melanopogon (fig. 1). Lizards of the species-rich genus Draco use large extendible dewlaps for communication, that differ in colour pattern and size between species – in a similar fashion to the anoles.

Figure 1 A. Male D. melanopogan, dewlap naturally extended (image a still from behavioural trials) and the angle of dewlap extension as measured from still; B. robot, dewlap treatments (Bi) solid colour and Bii) two-coloured); and C. artificially extended dewlaps of a male and female D. melanopogan.

To test whether the dewlap colour and pattern function more to facilitate 1. signal detection and 2. conspecific recognition, we presented free-living lizards with robots displaying dewlaps of six different designs, varying in the proportion of the black and white components.

In this case, our robots were just ‘visual flags’ that mimicked the dewlap size and shape, as well as the speed and display pattern of live Draco melanopogan lizards (video 1). Having only the dewlap / visual flag and not the rest of the lizard body allowed us to look solely at the salience of the dewlap colour and pattern itself – without adding any identifying or qualifying information in the form of a body.

Video 1: ‘The floating dewlap’

Our experiment had six colour treatments ranging from “natural” (population typical design, fig. 1) to unnatural (wrong colour, no pattern) – and from very conspicuous (high internal contrast and high contrast against the background for each colour) to very inconspicuous (matching the luminance of the background). Thus, we could test both the ‘detection’ and ‘conspecific recognition’ hypotheses with the same set of treatments.

Predictions for Hypothesis 1: We predicted that should the dewlap colour pattern function in signal detection, that more conspicuous dewlap treatments would be detected sooner than less conspicuous dewlaps. Each of the two-coloured treatments were more conspicuous than the single-coloured treatments, as they had the same high contrast black and white elements, but they also had the high internal contrast of the black against the white (75.02 JND). Provided the receiver has sufficient visual acuity at the viewing distance to be able to distinguish the two colours from one another, internal contrast increases signal conspicuousness, and the more equal the two adjacent colour patches are in size (i.e. 50% of the dewlap black – 50% of the dewlap white) the greater the internal contrast. There is no existing data on the visual acuity of Draco lizards, so for this experiment we stuck to the natural dewlap size and viewing distances, with small oscillations around the natural proportions of black and white.

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Along with Devi Stuart-Fox, Indraneil Das and Terry Ord, I recently published a paper in Biology Letters showing that arboreal Draco sumatranus lizards orient themselves on the tree trunk perpendicular to the position of the sun during broadcast signalling. This presumably increases the radiance of the translucent dewlap, and likely it’s conspicuousness.

Figure 1. (a) Draco sumatranus male displaying, showing the transmission of sunlight through the dewlap (photo: T. J. Ord). (b) Perch angle for displaying males, and (c) perch angle for non-displaying males, measured in relation to the sun. Both perpendicular angles (90° and 270°) have been transformed to equal 180°.

Draco lizards are ecologically analogous to the anoles and share similar signalling behaviour (see this recent Draco clip from the BBC’s Planet Earth II). They too possess extendable dewlaps that differ in colour and size between sex / species groups, and they also live in many different habitat types throughout Southeast Asia. I’ve written about my Draco research on Anole Annals before, here and here, if you’re interested – I hope they’re now well accepted as honorary anoles!

Like the anoles, the skin of the dewlap for many Draco species is stretched thin when extended and allows light to pass through.  Leo Fleishman published a Functional Ecology paper in 2015 measuring how the dewlap of Anolis lineatopis appears to glow when positioned with the sun behind them, and how this might improve signalling efficacy. Contrary to expectation, they found the transmission of light through the dewlap doesn’t improve the luminance contrast of the dewlap against the background. The radiance of the dewlap is increased by light transmission (radiance is the sum of the light reflected by the dewlap and any transmitted through the dewlap) – but patches of high radiance are very common in Anolis lineatopis forest shade environment, due to many the little shafts of light shining between gaps in the leaves. Instead they showed that due to the higher total intensity of the dewlap colour (thanks to light transmission) it’s probably easier for a conspecific to discriminate the signal from the natural background colours.

Given this and the similarity between anole and Draco dewlaps, I wondered whether Draco lizards might behaviourally adapt their position on the trunk relative to the position of the sun, to maximise the exposure of the extended dewlap to sunlight. To look at this, I just observed the position of the lizard relative to the sun upon first sighting, and noted whether the lizard was displaying, and if so, whether was it directly to a neighbouring conspecific, or whether it was a territorial broadcast display. We found males were significantly more likely to be oriented perpendicular to the sun when displaying, but not when not displaying (fig. 1).

Of course, signals intended for specific individuals in close-range encounters require the signaller to position themselves such that the receiver is in line of sight – but Draco lizards (and anoles) also give these ‘broadcast signals’ which are not intended for any specific individual, but just as territorial display. For these signals, where there is not another lizard around, they seem to orient themselves perpendicular to the sun, so their extended dewlap is exposed to the most light.

Female D. sumatranus also have dewlaps, but they are small in size and females only very occasionally engage in broadcast display.  I had not expected to see this orientation behaviour in females, as their dewlaps appear opaque and so don’t benefit from light transmission. However, I found the same orientation pattern for females as for males: perpendicular to the sun when displaying, but not when not displaying. This is perhaps because their dewlap reflects UV light (fig. 2) and direct sunlight is richer in UV and shorter wavelengths than light reflected off objects in the surrounding scene. Males have yellow dewlaps, and they too reflect a little UV (though much less than females). Of course, the transmission of light is unidirectional and only increases the radiance of the dewlap for those viewing the dewlap from the opposite side to that of illumination, so the benefit of direct sunlight hitting the UV/yellow male dewlap likely plays a role in this orientation behaviour for males as well.

Figure 2. a) Draco sumatranus male yellow dewlap colour reflectance;
(b) Draco sumatranus female blue dewlap colour reflectance.

A new study out in Biology Letters by myself, Devi Stuart-Fox, Terry Ord and Indraneil Das found that two populations of the same species of gliding lizard – Draco cornutus – have diverged in gliding membrane colouration to match the colours of falling leaves in their respective habitats. An Anole Annals post by Ambika Kamath earlier this year looked at the study briefly after we’d spoken at the Animal Behaviour Conference in Princeton, but I thought I’d elaborate a little on working with Draco and how we devised the falling leaf camouflage hypothesis.

Figure 1. Draco cornutus at Bako National Park (photo credit– Devi Stuart-Fox)

Draco are small arboreal agamids, found throughout South-East Asia. They have extendable gliding membranes that they use for gliding between trees in their habitats. They also have dewlaps – like the Anoles – used in broadcast display to communicate with conspecifics. My work generally focuses on the diversity in dewlap colouration among species and how differences in habitat influence signal efficacy and may lead to speciation. This involves measuring the colours of lizards as well as taking behavioural footage of individuals of different species to look at how the patterns of display differ.

httpv://youtu.be/I_oeY9cIWOg

Footage by Terry Ord

Most Draco are very difficult to spot as they are well camouflaged and perch at least 3 metres high in their trees. Given this, searching for movement or displays are the best ways to locate an individual. Walking through the forest, we would often see in our periphery what we would initially dismiss as a falling leaf, only to later discover it was a gliding lizard. Indeed we quickly learnt to focus on ‘falling leaves’ when on the lookout for Draco and this was quite a fruitful approach. Indraneil Das was the first to suggest the gliding membranes were coloured to look like falling leaves – but it was a couple of years until we started to think about how we might test the idea. It became difficult to ignore how similar the fallen leaves on the ground at various study sites so closely resembled the colours and patterns of the gliding membranes of Draco species living in those immediate areas.

Then we made to trip to Niah Caves National Park in northern Borneo and came across a second population of D. cornutus.

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A recent study in Oecologica by Terry Ord and myself found striking parallels in habitat use and morphology between the phylogenetically distinct Anolis and Draco genera.  Draco (family: Agamidae), for those who don’t know, is a genus of gliding lizards found throughout southeast Asia that are similar to anoles in that they communicate with conspecifics using bright and diversely coloured dewlaps (see picture).

(L: Draco sumatranus; R: anole)

A defining characteristics of anole ecology is their ecomorphology – a description of the species microhabitat and its morphological adaptions for thriving there. Anole species living sympatrically avoid interspecific competition by partitioning their habitats and resources, and consequently develop morphological adaptations that are suited to their slice of the habitat. As Draco species are also often found in sympatry, we tested whether competition pressures had resulted in similar habitat partitioning and corresponding morphological characters (or ecomorphs). Whilst it’s perhaps a bit early to suggest that Draco have  evolved the full complement of anole ecomorph classes, the Draco taxa studied largely clustered into two groups that shared characteristics with the Greater Antillean anoles. The figure below (panel b) shows a combined Draco/anole phenogram, based on morphology and ecobehaviour (the anoles are labelled only by ecomorph). The Draco species fall out largely in line with groups of ‘trunk-ground’ anoles towards the top of the phenogram, and ‘trunk-crown’ anole towards the bottom.  

One of the better diagnostic features of the Greater Antillean anole ecomorphs are the differences in perch use and subsequent differences in limb length. The plot below shows total hindlimb length (size-free residuals) of adult males of Draco species and Greater Antillean anoles, as a function of perch circumference.  The relationship between limb length and perch size is nearly identical between the groups, with a very similar slope, and only a difference in y-intercept owing to differences in body length (Draco bodies are elongated to accommodate gliding membranes).  The same unit increase in perch size results in the same unit increase in limb length for both genera.

These results are surprising considering that this relationship has not been found in species that are more closely related to the Greater Antillean Anolis (see study for references) and because Draco and Anolis have very different ‘key innovations’ for locomotion in their respective habitats (toe pads for Anolis and gliding membranes for Draco). This implies that Draco species have experienced interspecific competition over resources in similar ways to the anoles, resulting in homologous character displacement.