Theory suggests that animal signal structure will have phylogenetic determinants, be constrained by morphology and physiology, and influenced by the environment in which signaling takes place. The structure of present day signals can be historically contingent such that related species share characteristics that differ from more distantly related species, but also that the capacity for evolutionary divergence is constrained by the ancestral state (Ord et al., 2011; Ord, 2012). Morphological differences will dictate the kinds of signals that animals can produce. For example, body size constrains acoustic structure in mammals (Reby and McComb, 2003), amphibians (Ryan and Brenowitz, 1985) and insects (Lubanga et al., 2016), while physiological limitations of visual threat displays are related to signal performance (Brandt, 2003). The environment in which signaling takes place is also a major contributor to signal diversity. Differences in microhabitat structure lead to variation in signal structure within species (acoustic signals: Hunter and Krebs, 1979; visual signals: Ramos and Peters, 2017a), while a/biotic noise will lead to long term (Slabbekoorn and Smith, 2002) and short-term changes in signal structure in a variety of signaling systems (Brumm, 2014), including acoustic (Slabbekoorn and Peet, 2003; Slabbekoorn, 2013) and visual (Ord et al., 2007; Peters et al., 2007) signals. What is sometimes difficult to determine is the relative contribution of environmental effects to variations in signal structure within and between species.

The influence of morphology and physiology on signal diversity can often be determined in a straightforward manner by relating specific traits to morphological measurements (Podos, 2001; Podos and Nowicki, 2004) or calculating energetic costs (Vehrencamp et al., 1989; Hoback and Wagner, 1997; Matsumasa and Murai, 2005; Stoddard and Salazar, 2011). Similarly, as closely related species are more likely to exhibit similar traits, the influence of phylogeny is now routinely examined by controlling for shared ancestry in the statistical model using phylogenetic comparative methods (PCMs; Ord and Martins, 2006; Turner et al., 2007). In contrast, environmental effects on signaling are more difficult to quantify and disentangle from morphological and phylogenetic constraints. Consequently, a useful way to consider the relative contribution of habitat characteristics and environmental effects is to select closely related species to minimize variation in phylogeny and morphology/physiology. Our understanding of environmental influence for some signaling modalities, such as sound and static visual signals, has progressed greatly with the use of playback experiments, and specialized tools like sound spectrographs and spectrophotometers (Morton, 1975; Ryan et al., 1990; Leal and Fleishman, 2004; Cocroft and Rodriguez, 2005; McLean et al., 2014). However, less information is available for motion-based visual displays as relevant environmental effects are more complex to quantify (Ramos and Peters, 2017b).

Dynamic visual signals are common in lizards and are used in a variety of contexts including male-female interactions (Peters et al., 2016), predator avoidance (Hasson, 1991), and territorial defense (Carpenter, 1978). Displays produced to defend a territory are particularly useful to lizards as they allow rivals, usually males, to assess each other from a distance and avoid physical confrontations (Peters and Ord, 2003). Color-based visual signals, which are also common among lizard families (Stuart-Fox and Ord, 2004), often require movements to expose brightly colored parts of the body, such as throat, dewlap, chest or abdomen (Mitchell, 1973; LeBas and Marshall, 2000; Stuart-Fox and Moussalli, 2008; Fleishman et al., 2009; Teasdale et al., 2013). The motor patterns involved in motion-based displays vary between species, but they often include dewlap extensions, head bobs, limb waves, tail flicks, or push ups (Carpenter, 1962; Carpenter et al., 1970; Purdue and Carpenter, 1972; Ord and Martins, 2006; Ramos and Peters, 2016).

The detection of lizard displays can be affected by the surrounding environment, as receivers need to filter out irrelevant environmental motion noise (Fleishman and Persons, 2001; Leal and Fleishman, 2002, 2004; Peters and Evans, 2003a; Peters, 2008). In the case of motion-based signaling lizards, the main source of motion noise is wind-blown plants (Fleishman, 1986; Peters and Evans, 2003a). Thus, motion-based signals are most effective when they stimulate the visual system of receivers in a way the noise environment does not (Fleishman, 1992). This means that the motion produced by the signal needs to contrast with the motion generated by the plants surrounding it (Endler, 1991; Fleishman, 1992; Peters et al., 2007; Bian et al., 2019). Additionally, the noise environment is site specific as it stems from the individual plants present and the topography of the area (Peters et al., 2008; Peters, 2013). Consequently, local adaptations to overcome noise and enhance signal efficacy should be expected in species occupying structurally distinct habitats. Within species variability of this kind has been observed (Ramos and Peters, 2017b), but data across species are limited.

We wished to examine whether environmental effects can be detected across multiple Australian agamid lizard species, controlling as much as possible for shared ancestry and differences in morphology. There are 14 genera of agamid lizards in Australia (Wilson and Swan, 2017), from which Ctenophorus is the most diverse (N = 29; McLean et al., 2013; Wilson and Swan, 2017; Dong et al., 2021) and has the highest number of known signaling species (N = 18; Ramos and Peters, 2016; Dong et al., 2021). Some of the most interesting species within the genus in terms of their social behavior belong to the Ctenophorus decresii complex, which consists of six closely related species (Figure 1; McLean et al., 2013): the tawny dragon (C. decresii), the peninsula dragon (C. fionni), the Barrier Range dragon (C. mirrityana), the swift rock dragon (C. modestus), the ochre dragon (C. tjantjalka), and the red-barred dragon (C. vadnappa). A recent study elevated the two lineages of C. decresii into distinct species, C. decresii as the southern lineage (Mount Lofty Ranges, Fleurieu Peninsula and Kangaroo Island in South Australia; Dong et al., 2021) and C. modestus as the northern lineage (Flinders Ranges and Olary Ranges, in South Australia; Dong et al., 2021). These species are sexually dimorphic, and the males usually display bright and conspicuous coloration during the breading season (Gibbons, 1979; McLean et al., 2013). They are also very similar in size, with C. tjantjalka possessing the smallest snout vent length (73 mm; Wilson and Swan, 2017) and C. decresii the largest (96 mm; Wilson and Swan, 2017). All members of the complex are dorsoventrally flattened and long-limbed; both of which are adaptations to their rocky habitats (for detailed descriptions of all species in the complex see Gibbons, 1977; Gibbons, 1979; Johnston, 1992; McLean et al., 2013; Dong et al., 2021). The six species in the C. decresii complex are territorial, and perform aggressive stereotyped motion displays against intruders (Gibbons, 1979; Osborne, 2005; McLean et al., 2013; Ramos, 2017). These displays can be divided in three sequential phases (Gibbons, 1979): lowering of dewlap and limb waves, hind leg push ups with tail coiling and head bobbing. While superficially similar, the displays performed by three members of the complex have been reported to differ both inter- and intra- specifically in speed, amplitude and number of repetitions of individual motor patterns (Gibbons, 1979). Additionally, it has been suggested that these differences could aid in taxonomic differentiation at the species level (Gibbons, 1979).

Our aim was to explore the signaling behavior of the C. decresii complex to determine whether potential environmental differences would be manifested as differences in signal structure. Our fieldwork preceded the recent reclassification of C. decresii and thus focuses on 5 of the 6 species (excluding C. decresii). This is an ideal group to examine this aim as they are closely related, morphologically similar and utilize signals that are superficially the same. However, they occupy slightly different microhabitats, and their signals have not been subjected to detailed analysis or comparison. Consequently, we address our aim by asking three underlying questions:

Our work was undertaken in the field and involved locating and filming unrestrained wild animals in situ, then carefully documenting the microhabitats in which signaling takes place. We have combined broad level analysis of the temporal structure and use of male territorial displays, with detailed quantification of displays following the approach described by Ramos and Peters (2017b), which involves reconstructing lizard display motion in three dimensions (3D) and comparing it to the noise environment to calculate signal contrast. By recording the signals and the relevant features of the noise environment independently, we are able to assess the performance of each species at the habitats of the other members of the C. decresii complex without physically translocating the lizards. We hypothesize that signaling displays will reflect the shared ancestry of the five species to some extent, but the details will differ in a manner that is linked to local signaling conditions.

Results of the present study confirm that the motor pattern repertoire employed during the territorial displays of species in the Ctenophorus decresii complex are almost indistinguishable from each other, as previously reported by Gibbons (1979) for C. modestus (as C. decresii), C. fionni, and C. vadnappa. We consider the implications of our findings below, although we acknowledge that our sample size for two species is low (N = 1 and 2). We made concerted efforts to locate and record the visual displays of all species, but information on the behavior of most Australian dragons is very limited (Melville and Wilson, 2019), which hampered efforts to locate and film natural behavior. Consequently, we acknowledge below when our interpretations are more speculative because of limited data.

The general design of the displays does not seem to differ. However, upon closer inspection, motor pattern use does appear to vary. The coefficients of variation indicate that head bobs, and to a lesser extend push ups, are employed differently by all species (Table 2). This variation in the use of motor patterns appears consistent with their phylogeny, particularly in terms of the number and duration of the components (Figure 4). Ctenophorus modestus, C. fionni and C. vadnappa are more similar to each other (Figure 4). Ctenophorus modestus and C. vadnappa also produce the highest motion speed averages (Figure 5), but in this regard, variation does not occur as neatly along phylogenetic lines. Instead, display speed is fastest in species found in the most planted habitats (Figures 5, 6). Thus, the potential masking effect of environmental noise is high in the habitats of C. modestus and C. vadnappa. This is also true for C. fionni, but in the case of this species, it is likely attributed to slow display speeds (Figure 5), short S-P distances (Figure 6), or both. Consequently, the Ctenophorus decresii complex might be an example of closely related species, retaining ancestral behavioral traits that have been modified to suit their specific habitats.

Results from the signal-noise contrast analyses revealed that displays by C. fionni are more susceptible to environmental noise in all habitats, while C. vadnappa displays are the least affected in each habitat. This was expected given that C. vadnappa produced the fastest motion speed averages. Gibbons (1979) determined that the push ups produced by C. vadnappa had greater amplitude than the equivalent motor patterns from C. modestus and C. fionni. Greater amplitudes can translate into faster speeds if the time intervals are kept equal, which indicates similarities between both studies.

Signal contrast can be used to assess the performance of motion signals and also to infer differences across habitats in the production of noise, as explained by Ramos and Peters (2017a,b). All species seem to perform much better when their signals are considered at the habitats of C. mirrityana, which suggests the noise environment at these sites are less likely to mask the signals produced by the lizards (Figure 7). Although we only recorded at two sites for this species, our findings can be partially explained by looking at the distribution of vegetation at these sites and the surrounding area. Ctenophorus mirrityana habitat not only contains a low density of relevant plants, but the signaler-plant distance average was almost as high as in C. modestus and C. vadnappa habitat (Figure 7). These two traits combined seemed to promote effective signaling in this habitat for all species. The sites utilized by C. fionni for signaling contain an even lower plant density, but this species also displays the shortest signaler-plant distance average of all lizards in the study. This means that C. fionni lizards do not often encounter plants during their territorial displays, but when they do, they signal in very close proximity, and this has consequences for motion segmentation by receivers. As such, despite superficially looking like the ideal signaling location (i.e., mostly large, flat rocks, and scarce vegetation), contrast scores are lower in C. fionni habitats. Overall, the potential for noise and signal masking in the habitats of C. modestus and C. vadnappa is high, but the species manage to perform relatively well according to our data. Signaling faster might be a way for these two species to offset the masking potential. As signaler-plant distances are smaller for C. fionni, attempts to signal faster against plant motion to improve contrast would be less effective (see Peters, 2013). Given the high speeds produced during their displays, it is not surprising that C. vadnappa performs best in all habitats compared to the other four species. Due to the nature of the fieldwork and the restricted and/or inaccessible distribution of some species, the sample sizes between species were inconsistent. Therefore, the results relating to comparisons of all five species should be taken with caution. This could explain the similarities between the convex hulls for C. modestus, C. fionni, and C. vadnappa, although our personal observations of the habitats for all species match well the sites that we sampled. It is also important to mention that despite the small sample size for C. tjantjalka, signaling in this species was reported in the literature for the first time in previous work (Ramos and Peters, 2016), but never recorded in free living lizards until now.

The results of this study suggest that there are signaling differences observed between species in this complex that are consistent with the notion of adaptations to the local environment. However, variation in the use of head bobs does appear relevant in a different context. Gibbons (1979) suggested that several aspects of the head bob motor pattern could have a species recognition function and could also be employed to taxonomically differentiate the species in the complex. While the current study focused on other display characteristics and used a different approach to analyze motion signals, we also identified variation in head bob use, particularly in the average duration and number of bobs performed per display in C. mirrityana. This is not surprising given that the species is the most phylogenetically distant in the complex (McLean et al., 2013). Ctenophorus mirrityana has only recently been described and was not included in Gibbons’ study, but variability in head bob use in our limited sample seems to be consistent. Nonetheless, species recognition might only be relevant for some populations of C. modestus and C. vadnappa that actually occur in sympatry. Gibbons (1979) identified the angle of the tail coil during the push up display as the most likely element for species recognition, and described it as vertical for C. vadnappa and horizontal for C. modestus (as C. decresii) and C. fionni. We did not observe the same pattern in the present study (data not presented). Instead, we compared other aspects of their signaling behavior and habitat. While we did not specifically look for differences between C. modestus and C. vadnappa, our results are mostly consistent with local adaptations and do not provide evidence that signaling behavior has a species recognition function. Historically both species were sympatric in some of our study sites as late as the mid 1970’s (Gibbons, 1979), but there currently does not seem to be an overlap in their distributions at these areas. Further studies on potential species recognition cues should target populations occurring in sympatry and therefore more likely to be influenced by the selective pressure of ensuring species recognition, and to show more obvious divergence in behavior.

Tail flicking behavior is yet another aspect worth exploring further. This motor pattern has been observed in all five species, however, according to our observations it is rarely included in the displays. In A. muricatus, most territorial displays are preceded by tail flicking, which tends to have a duration of several seconds (Peters and Evans, 2003b). In contrast, members of the C. decresii complex perform tail flicks infrequently and briefly. This might be related to the specific structure of the tail flicks, and if they are actually required to attract the attention of receivers and enhance signal efficacy, or it could be a remnant from an ancestral behavior. Regardless, it might be interesting to specifically analyze the function and structure of this motor pattern in the context of the noise environment.

Although there clearly is an effect of shared ancestry, our data provides evidence that members of the C. decresii complex exhibit adaptations in their signaling behavior to the local characteristics of their habitat. Some of these adaptations may also aid in species recognition, but our results are not conclusive in this matter. Many avenues of research remain untested in this group, such as the inclusion of C. decresii in the analyses, detailed studies of sympatric populations, and sampling of multiple populations for the wide-ranging C. modestus and C. fionni, although we are already taking the first steps (Wilson et al., 2021). Clearly, habitat structure can differentially influence the signaling behavior of closely related species with similar general signal design and morphology, which are likely a consequence of the ancestral state.

The raw data supporting the conclusions of this article will be made available by the authors, without undue reservation.

The animal study was reviewed and approved by the La Trobe University Animal Ethics Committee and Wildlife Ethics Committee, South Australia.

JR and RP designed the experiment, analyzed the data, and wrote the manuscript. JR conducted the experiment and collected the data. Both authors reviewed and approved the manuscript.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.