Nature's headlamps: A unique light-focusing structure in Parasesarma de Man, 1895 mangrove crabs

Abstract

Colors are used extensively in animal visual signaling, playing an important role in camouflage, aposematism, mate recognition and choice, and intrasexual competition (Laidre & Johnstone, 2013; Pérez-Rodríguez et al., 2017). In many cases, animals should benefit from being able to augment the intensity of the visual signals they transmit (Osorio & Vorobyev, 2005), especially in low-light environments such as mangrove forest undergrowth and the deep sea. During multiple mangrove fieldtrips, we observed that the pigmented facial bands of the crab Parasesarma eumolpe de Man, 1895, were particularly eye-catching. This common Indo-Pacific crab bears two colored facial bands on the anterior surface of its body, each approximately 6 mm in width and 1.6 mm in height (Figure 1A). Previous field and manipulative studies have shown that the colors of these bands differ between sexes, with more blue reflected by bands of males compared to females (Huang et al., 2008). Pigments are known to be derived from carotenoids in the crabs' diet, fading when the crabs are starved and brightening when they are fed, suggesting they provide a cue of physical condition (Todd et al., 2011; Wang & Todd, 2012). Finally, the bands are used in both intersexual signaling and intrasexual competition, affecting sex recognition and resource holding potential (Todd et al., 2011).

However, this past research did not explain the anatomical basis of the exceptional facial band brightness we saw in the field. Understanding the mechanism of this brightness, potentially micro- or macro-morphological features, could help in determining the function of the crabs' facial bands, for example, whether they are used for communication with conspecifics or otherwise, and thereby shed light on its evolution by pinpointing the trait that has presumably been selected for. Here, we demonstrate that the concave macrostructure of these bands acts in a manner analogous to the reflector of a headlamp, increasing their apparent brightness at the same range of angles that are optimum for signaling between two crabs. Scanning electron microscopy (SEM) indicated no iridescence or structural coloration (Figure 1B; Appendix S1: Figure S1). These facial bands are, to our knowledge, the first example of light-focusing, external, macro signaling structures in animals.

We first modeled the typical signaling behavior of P. eumolpe (Figure 1C) by recording interactions between crabs (30 male and 26 female) in situ at Mandai Kechil mangrove in Singapore. Crabs were observed from 5 to 10 m away using binoculars. A reference scale (usually a short ruler) was placed in the vicinity of the crabs so distances could be estimated. A pair of crabs was considered to be interacting when they both stopped traveling over the substrate, faced each other, and began to observe and/or respond to each other. We measured (1) the eye stalk length, L, of the crabs: 4.46 ± 0.58 mm (mean ± SD) in males and 3.96 ± 0.34 mm in females; (2) the average crab body angle during interactions, θ_c: 30°; and (3) typical interaction distances, D: 50–500 mm. We then calculated for the range of interaction distances observed.

To test the hypothesis that P. eumolpe facial bands focus and reflect light at the same range of optimum angles, we used customized probe holders and an Ocean Insight Jaz reflectance spectrometer to illuminate the crabs' facial bands (10 males and 10 females) from incident light angles, θ_i, from +0° to +60° (at 5° intervals). For each incident angle, we measured the intensity of the light reflecting off the facial bands toward the receiving probe (also at 5° intervals). In both males and females, the intensity of the light reflected by the bands generally peaks at +0° or +5° (Figure 2). This coincides with the optimum angles for reflected light predicted by our intraspecific interactions model (Figure 1D) and suggests that the structure of the facial bands focuses reflected light to enhance the bands' brightness for signaling between conspecifics.

To investigate the mechanism that produces this effect, we created a 3D computer model of how light reflects off the facial band's surface (Figure 1E) using the Lightwave 9.6 program. High-resolution texture images were mapped via frontal projection onto a 3D geometric mesh surface generated with a non-contact 3D scanner (Figure 1E). The resulting model was used to simulate 10 different virtual lighting conditions. In each scenario, illuminating light was provided from a single incident angle (from −60° to +60° inclusive at 15° intervals); the paths of the light rays reflecting off the facial band surface were modeled, and the appearance of the crab from the 0° angle was generated. This model showed that the facial bands directed most of the reflected light toward the 0° angle, regardless of incident light angle (Figure 1F). In addition, we determined that the facial band is not iridescent (Appendix S1: Figure S1) and that its color is unlikely to be caused by structural coloration as SEM revealed no distinctive microstructures (Appendix S1: Figure S2). However, it remains possible that these exist within or below the cuticle, and further exploration using techniques such as holographic microscopy, freeze/fracture SEM, or transmission electron microscopy should be able to confirm this. Together, these findings suggest strongly that the ability of the bands to focus the light they reflect at the optimum angle for conspecific signaling is due to the macrostructure of the facial bands—akin to the brightness of car headlamps being increased by the curved reflective surfaces behind the bulbs.

Given the ability of the facial bands to focus reflected light at the optimal angles for signaling, we investigated whether their brightness and their striking pigment-based hue (blue in males and green in females; Appendix S1: Figure S3A,B) (Wang & Todd, 2012) may influence the crabs' ability to communicate using their facial bands. To test the role of brightness alone, we presented P. eumolpe crabs with a choice between two images: one with a bright facial band and another with a dull facial band (with 62% the luminance of the bright band, the average luminance when the band is viewed from outside the +0° to +5° range). Both male and female test specimens were observed to preferentially approach image stimuli with brighter bands (Figure 3A) (males, 20 trials, one-sided p < 0.01; females, 17 trials, one-sided p < 0.01; there was no significant difference between the response of the two sexes, p = 0.26). Negative controls (crabs were placed into chambers without stimuli) confirmed that the crab specimens in our trials were actively making a choice (Figure 3B): when placed into a trial chamber without any stimuli, most specimens remained within the compartment where they were inserted and did not make any choice (N = 96, one-sided p < 0.001). Our results suggest that greater facial band brightness, which the macrostructure has a positive effect on, enhances the crabs' ability to transmit visual signals.

We further hypothesized that the colors of the facial bands, independent of their brightness, may play a role in how the crabs communicate. To test this, both male and female P. eumolpe crabs were used as test specimens (i.e., “choosers”) in two choice experiments employing V-shaped chambers (Chan et al., 2020). In the first experiment (Figure 3C), they chose between two images of androgyne crab bodies (created by interposing images of both sexes to eliminate sex-specific visual cues on the body) bearing either male- or female-specific facial band colors (see Huang et al., 2008; Appendix S1: Figure S3). In the second experiment (Figure 3D), they selected between two live crabs of different sexes as a positive control. In both experiments, specimens preferentially approached stimuli of the same sex. Male crabs preferred images with male-colored facial bands and female crabs preferred images with female-colored facial bands (N = 67, p < 0.001). Similarly, male crabs preferred male live crabs and female crabs preferred female live crabs (N = 67, p < 0.001). These findings indicate a role of facial band color in signaling and raise the possibility that increased facial band brightness, beyond conveying information in and of itself, may also help to make P. eumolpe facial band colors more visible in order to enhance communication between individuals.

Diet-based carotenoids are used to produce the colors in P. eumolpe facial bands (Wang & Todd, 2012), and we show here that this color, which is different in male and female crabs (Huang et al., 2008), is involved in conspecific signaling (also, see Todd et al., 2011). Our data further demonstrate that differences in facial band brightness alone are sufficient to elicit a behavioral response. Our results, in combination with those from previous works in the field (e.g., Huang et al., 2008; Todd et al., 2011; Wang & Todd, 2012), suggest that the crabs are able to use both color and brightness components of visual signals as separate sources of information (e.g., to reinforce one another or for different purposes altogether), adding to the growing evidence for complex, multi-component signals in animal communication (Hebets et al., 2016; Ratcliff & Nydam, 2008; Tibbetts et al., 2020). However, many questions remain, such as exactly what information is being conveyed by each component (e.g., sex identification versus fitness or health level), what effect smaller changes in brightness may have (Endler, 1987), and whether other visual properties may also play a role (Chan et al., 2019). It remains unclear exactly what roles color and brightness play in communication within this species and whether their effects may interact with each other (e.g., see Lim et al., 2019) or with information conveyed over different signaling modes (e.g., stridulation has been documented in Parasesarma crabs; Boon et al., 2009). It is also interesting that the P. eumolpe crabs in our study were attracted to facial band colors representing the same sex, whereas crabs of a closely related species, Parasesarma peninsulare, were attracted to the opposite sex (Chan et al., 2020). These results will inform future studies on the role or roles of the brightness and colors of the facial bands in signaling—for example, to attract conspecifics as mates, to repel them to defend territory, or to deter predators—and on how these roles may vary among different species in their natural environment.

Considering the potential benefits of using light-focusing, reflective macrostructures (such as the facial bands we describe here) to enhance animal visual signals, it is somewhat surprising that such structures are not more common in nature. It may be that, in most animals, it is more effective or efficient to amplify a transmitted signal by expanding the area it covers (e.g., the entire body of the red seven-spot ladybird Coccinella septempunctata forms its aposematic signal; Brakefield et al., 1994) rather than by modifying the structure of the existing signal-bearing area. Alternatively, it could be more beneficial for animals to bear structures that improve signal detection rather than transmission. A good example is the tapetum lucidum (the layer of reflective tissue responsible for eyeshine in animals such as cats), which is functionally similar to the facial bands here (i.e., it also focuses the light it reflects), but it is instead used to enhance night vision in a wide range of animals (e.g., teleost fish, crocodilians, elasmobranchs, cetaceans, carnivores, ungulates, and some arachnids) (Ollivier et al., 2004). It is conceivable, however, that the same structure could be used by an animal both as a visual signal and a sensory enhancement (e.g., the luminescent organ in the pupils of flashlight fishes; Howland et al., 1992). Finally, it may be more efficient for signal transmitters to simply move closer to the intended recipient.

The nature of the mangrove habitat in which these Parasesarma crabs are found is likely to have played a role in the development of their facial bands. The dull brown colors of the mangrove substrate (which differ distinctly from the crabs' bright blue and green facial bands; Huang et al., 2008) and dim lighting conditions in the undergrowth, coupled with the existence of safe hiding places from which to signal (e.g., root structures and leaf litter) and a marked predation risk when leaving these refuges (Wilson, 1989), could have created the specific pressures required for the facial bands to evolve. Hence, there may be other examples of similar structures in species inhabiting other low-light environments (where they offer the greatest advantage in signaling) with high but heterogeneous predation pressures, such as the undergrowth of inland tropical rainforests and aquatic benthic zones near the limits of sunlight penetration, which are typically less well studied and where many animals potentially remain undiscovered.

In summary, we demonstrate how the macrostructure of P. eumolpe facial bands focuses the light they reflect toward the same range of angles that are optimal for transmitting visual signals to conspecifics. We further show that the colors and brightness of the bands are used to communicate between conspecifics, suggesting that the light-focusing effect we describe functions to enhance visual signals in P. eumolpe.

Conceptualization: Peter A. Todd. Methodology: Peter A. Todd, Zuze Boh, Hui Shan Soh, Huiwen Huang, and Wendy Yanling Wang. Investigation: Zuze Boh, Hui Shan Soh, Huiwen Huang, Peter A. Todd, and Wendy Yanling Wang. Formal analysis: Zuze Boh, Hui Shan Soh, Huiwen Huang, Wendy Yanling Wang, and Ian Zhi Wen Chan. Data curation: Ian Zhi Wen Chan. Writing—original draft: Ian Zhi Wen Chan. Writing—reviewing and editing: Peter A. Todd and Ian Zhi Wen Chan. Supervision: Peter A. Todd. Resources: Peter A. Todd. Funding acquisition: Peter A. Todd. Authors are listed in order of decreasing contribution to this work.

The authors declare no conflicts of interest.