by Darren McPhee, John Keep, Kay Watty, Chris Murphy and Kirsten Slemint
BACKGROUND, AIMS & HYPOTHESIS
Both vertebrates and invertebrates are well known for displaying varying degrees of intra- and interspecies communication differing in the underlying mechanisms and complexity. One method of communication obvious to humans is aposematic or warning display behaviour. Aposematic communication is a behaviour that relies on a display of colours and patterns to deter predators and competitors and acts as a warning that the displaying individual is either dangerous or distasteful (Skelhorn et al., 2016). This behaviour is found across a diverse range of species, however, is especially common in invertebrates such as crustaceans. By investigating the visual ecology of organisms and how they perceive their environment, scientists have been able to deconstruct and better understand the mechanisms that drive these display behaviours.
Research analysing an organism’s interaction with their environment through visual cues has been extensive. This is mainly due to the interest in quantifying the differences in visual capabilities when compared to humans. Some animals are only capable of detecting the difference between light and dark or the actual direction light is coming from. In contrast, others have developed highly complex eyes which enable them to create sharp and colourful images. This complexity of image processing allows them to more effectively interact with their environment and other individuals.
Colour vision forms a large part of the research that investigates the visual ecology of organisms. This has been driven in part by the fact that these display behaviours often operate within the spectrum of observation that humans are adapted to (Laidre and Johnstone 2013). However, recent technological advancements have allowed us to expand research into sensory spectrums beyond historical comprehension (How et al., 2012).
The importance of these differences between human and animal colour vision becomes clear when observing examples in nature. Invertebrates, for example, display vast variations in the colouration of their chitinous exoskeletons (Cuthill et al., 2017). Some might seem dull while others appear spectacular, generally driven by underlying behavioural influences.
Almost all birds are tetrachromats, meaning that they possess four different cues for detecting colour whilst humans only possess three. Further to this, birds have photoreceptor sensitivity that reaches into the ultraviolet (UV) spectrum (Bennett et al., 1994). Consequently, the colouration of their plumages might appear significantly different to other birds than it does to us, producing different visual cues depending on the observer (Hausmann et al., 2003). This is not only limited to vertebrates, as a number of invertebrates are known to possess highly developed visual systems which enable them to view their environment with a broader range of vision (Menzel 1979). Mantis shrimps, or Stomatopods, are a good example to observe because not only are they capable of detecting UV light but they can also process information coming from polarized light (Marshall and Oberwinkler 1999).
Fiddler crabs are common brachyuran decapod crustaceans, belonging to the family Ocypodidae of the genus Uca (Zeil et al., 2006). They are adapted to warm climates and typically inhabit the intertidal zones of estuaries and sheltered bays (Davie 2011). There are a total of 62 species of fiddler crab in nine subgenera that are distributed widely throughout the tropics and subtropics around the world. Australia has 18 of the total species, 12 of which are known to be endemic (Davie 2011). Depending on their distribution the activity of populations varies under different environmental conditions. They are reproductively active throughout the year in the tropics but are restricted to mating in the dry season in the subtropics (Crane 1975).
Fiddler crabs are well known for displaying aposematic behaviour, waving their claws as a warning signal. This makes them a well-suited model for investigating the significance of visually driven environmental parameters that influence behaviours (Layne et al., 1997; Detto and Blackwell 2009). Males and females are easily differentiated as males possess an enlarged cheliped, which frequently features in their display behaviour (Zeil et al., 2006). Male-male aggression is observed almost constantly in fiddler crabs. They wave their enlarged cheliped in the air to intimidate other males, maintain their territory, and to display dominance and fitness to potential mates. Evidence suggests that females of the species Uca tangeri are more likely to approach males with larger and more raised claws than those with smaller and lowered claws (Oliveira and Custódio 1998). Moreover, claw size has been directly linked to burrow quality which is a determining factor of fitness when females are choosing a potential mate (Latruffe et al., 1999).
Aside from the obvious visual cue of the enlarged claw, studies into the signalling behaviour of Uca mjoebergi showed that the enlarged claws reflect ultraviolet wavelengths of light that their dichromatic visual system allows them to detect (Detto and Blackwell 2009). The fiddler crabs visual system is highly adapted to living in the flattened world of an intertidal mudflat. Their compound eyes are placed on long stalks giving them a panoramic visual field enabling them to monitor their surroundings without much eye movement. They use retinal position as a distance cue because objects that are close to them will appear lower in their field of vision compared to things in the distance (Layne et al., 1997). The horizon, therefore, creates a social world below it and a world of predators above it. Although fiddler crabs have poor resolution, they can detect other crabs from about 2m away, humans on the mudflat from as far as a 100m away and predatory birds flying over them ~17m away depending on their size (Zeil et al., 2006).
Fiddler crabs are known to be highly sensitive to both UV and polarized light, with one of the highest known behavioural polarization sensitivities of all crustaceans (Zeil and Hemmi 2005; Detto 2007; How et al., 2012). The compound eyes of the fiddler crab Uca pugnax were found to have only one spectral class of visual receptor, with maximum absorption between 508 nm and 530 nm on the larger retinular cell (Jordão et al., 2007). However, this peak in spectral sensitivity is modified by coloured screening pigment vesicles that line photoreceptor cells. As a result of this, the sensitivity is shifted towards longer wavelengths that produce a clear sensitivity peak in the orange-red region of the light spectrum (Jordão et al., 2007). This sensitivity relates to the social signalling display behaviour of fiddler crabs in the form of claw waving. This inclination towards longer wavelengths in their visual system allows them to enhance the contrast between the colouration of the claw against the blue sky (Jordão et al., 2007). This reflectance at the 530 nm wavelength is visible to humans and is responsible for their colourful appearance. Similarly, there is another peak in reflectance at the 325 nm wavelength (UVA range), which is invisible to humans, but not to other fiddler crabs. Females have been found to preferentially select males with this level of reflectance over males that lacked ultraviolet reflectance (Detto and Backwell 2009).
Whilst the research into fiddler crab species has been extensive to date, the focus has primarily been on the behavioural influence of physical traits such as size, colour, and signalling behaviours. This same research concludes that the interactions between male fiddler crabs and the sexual selective behaviour of the female are highly influenced by these traits (Oliveira et al., 1998). Due to this, male-male interactions such as the aposematic behaviour of claw waving and the mechanisms that influence this have largely been overlooked.
Through this study, we aim to expand upon pre-existing knowledge on the interactions between male Orange-clawed fiddler crabs, Uca coarctata to determine whether male-male aposematic behaviour (claw waving) is significantly influenced by ultraviolet cues reflected off their enlarged cheliped. We hypothesise that males treated to reduce the UV reflectance of their claw will exhibit a decreased ability to communicate with neighbouring males. We predict that this will impact the males ability to defend his territory and increase the frequency of physical conflicts among neighbouring males.
SIGNIFICANCE OF STUDY
Research investigating visual ecology in relation to the behaviour of organisms has been significantly biased towards assessing colour vision capabilities, particularly towards human colour vision. In many cases, invertebrates found to possess colour vision have evolved intra-species specific behaviours in response to cues from within the visual spectrum of light (Menzel 1979; Marshall et al., 1996; Detto 2007; Jordão et al., 2007). However, in most cases, the influence of light outside the visual spectrum was not taken into account. Broadly generalising, the observed behaviours were driven by chromatic vision may potentially increase the likelihood of the behaviour being misinterpreted. This may occur if the behaviour is instead driven by cues outside of the spectrum visual to humans, yet interpreted as a response to a chromatic cue. Until recently, mate choice in fiddler crabs was primarily accepted to be driven by colouration of the male claw (Detto 2007). However, this behaviour was recently found to also be driven by ultraviolet cues, demonstrating the potential for misinterpretation of behaviours driven by visual stimuli (Detto & Blackwell 2009).
Through this study, we intend to form a more in-depth understanding of the influence of ultraviolet cues on the intra-species interactions between male U. coarctata fiddler crabs in Australia. If UV is found to significantly influence interactions between fiddler crabs, it may demonstrate an example of a potential trade-off between reflectance and the risks associated with broadcast signalling. Predators of fiddler crabs and other intertidal species have evolved adaptations that may facilitate the exploitation of ultraviolet cues displayed by prey (Honkavaara et al., 2002; Cronin 2005).
Displaying a highly reflective claw may increase the predation risk of those species adapted to perceive ultraviolet cues. Consequently, future research may seek to investigate whether there is a relationship between the level of reflectance and predation rates, giving insight into a potential coevolutionary model.
From a broader perspective, knowledge gained from this research may inform future research into the behaviours displayed by other related species of fiddler crabs in the Uca genus as these behaviours are very similar across species (Christy and Salmon 1984; How et al., 2008). Previous research on fiddler crab behaviours that did not consider the influence of UV reflectance may have missed crucial considerations for interpretation of their data. If UV reflectance is found to significantly influence behaviour, all future research on fiddler crabs and closely related species will need to ensure that this effect is taken into account.
RESEARCH PLAN & METHODS
The Orange-clawed Fiddler Crab, Uca coarctata, has been selected as the subject of this study due to its common occurrence in the Moreton Bay region. Observation and treatment of U. coarctata will be conducted during low-tide in their natural habitat on the intertidal mudflats of North Stradbroke Island, Queensland (27° 28′ 42.80” S, 153° 25′ 14.44” E). Prior to commencing research, a reconnaissance and pilot study will be undertaken to determine site suitability and population health. Reconnaissance will also serve to highlight any ethical and cultural considerations to ensure minimal disturbance to the site, its custodians and inhabitants. Following this, we aim to begin all observations and data collection within a two-month window commencing April 1st, 2018.
Experimental observations will centre around a randomly selected focal male. At approximately 2m, fiddler crabs are able to visually detect and identify other males so to account for this, a 4m2 quadrat will establish the area of observation (Zeil et al., 2006). All males from within the area of observation will be collected and have their physical characteristics (length, width and weight) recorded, taking note of the enlarged cheliped features (length, width and colour) whilst also establishing if the cheliped has been regenerated. Once captured and measurements recorded, all male subjects will have one of the following treatments applied to their enlarged cheliped. To avoid handling fatigue, a brush applicator will be used for each treatment.
1. Clear petroleum jelly (Vaseline) applied to control specimens;
2. Clear, ethanol free SPF (50+) sunscreen (suitable for children under 6 months) applied to treatment specimens
Clear substances (Petroleum jelly and sunscreen) were chosen to reduce the impact their application may have on the mechanism of colour recognition in signalling behaviour. Treatments will be adjusted to create two testing scenarios with the focal male receiving treatment and periphery males as control (Figure 1) or the inverse with the periphery males receiving treatment and the focal male as control (Figure 2).
Figure 1: Schematic of scenario one. A 4m2 quadrat outlines the area for observation where the focal male crab in red is treated with SPF (50+) sunscreen, while the periphery males in black have petroleum jelly (Vaseline) applied as control.
Figure 2: Schematic of scenario two. A 4m2 quadrat outlines the area for observation where the focal male crab in red has petroleum jelly (Vaseline) applied as control and the periphery males in black have SPF (50+) sunscreen applied as treatment.
Following application of treatment, male subjects will be returned to their original burrows. The subject’s behaviour will be observed by our research team and video footage will be remotely recorded on an elevated GoPro Hero4 camera. This footage will capture all behavioural interactions between the male subjects and serve to measure the distance travelled within the area of observation.
Interactions will be recorded as a categorical True/False variable for aggression (eg: fighting) following a Bernoulli distribution and analysed through the use of an ANOVA to test for statistical significance to the level of 0.05. While total area occupied / area of occurrence of the focal male away from his burrow will be recorded in each scenario as a proportion of the total area observed and analysed through a general linear model to test for statistical significance to the level of 0.05.
In order to measure an approximate spectral reflectance range for U.coarctata, we will analyse multiple live specimens from our observed population. The reflectance range of 5 specimens will be measured on a spectrophotometer under the direction of Dr Karen Cheney in the Visual Ecology Laboratory, School of Biological Sciences, University of Queensland, Brisbane, Australia.
Motion analysis software
To assess movement patterns of individuals throughout the area of observation, a motion analysis software program called “Kinovea” will be used. Multiple 30-min video recordings will be captured of each h scenario and following our observations, this footage will be fed into Kinovea where a semi-automated tracking tool will allow us to illustrate and compare the movement of individuals exposed to each treatment scenario.
If there is an effect of UV reflectance on the behaviour of male U. coarctata, we expect to see males treated with SPF (50+) sunscreen to experience increased levels of aggression from control males and an associated decrease in the distance the male treated with SPF (50+) sunscreen will be moved from his burrow.
Table 1: Potential outcomes and their implications from the proposed study evaluating behavioural response of Uca coarctata toward male competitors in the presence and absence of ultraviolet cues.
Bennett, A., Cuthill, I., & Norris, K. (1994). Sexual selection and the mismeasure of color. The American Naturalist, 144, pp.848-860.
Crane, J. (1975). Fiddler crabs of the world: Ocypodidae: genus Uca.
Christy, J., & Salmon, M. (1984) Ecology and evolution of mating systems of fiddler crabs (genus Uca). Biological Reviews, 59, pp.483-509.
Cronin, T.W. (2005). The visual ecology of predator-prey interactions. In Barbosa, P. & Castellanos, I. (eds.) Ecology of predator-prey interactions. Oxford University Press, pp.105-138.
Cuthill, I., Allen, W., Arbuckle, K., Caspers, B., Chaplin, G., & Hauber, M. et al. (2017). The biology of color. Science, 357, eaan0221.
Davie, P. (2011). Wild guide to Moreton Bay and adjacent coasts. South Brisbane, Qld.: Queensland Museum.
Detto, T. (2007). The fiddler crab Uca mjoebergi uses colour vision in mate choice. Proceedings of the Royal Society B: Biological Sciences, 274, pp.2785-2790.
Detto, T., & Backwell, P. (2009). The fiddler crab Uca mjoebergi uses ultraviolet cues in mate choice but not aggressive interactions. Animal Behaviour, 78, pp.407-411.
Hausmann, F., Arnold, K., Marshall, N, & Owens, I. (2003). Ultraviolet signals in birds are special. Proceedings of the Royal Society of London B: Biological Sciences, 270, pp.61-67.
Honkavaara, J., Koivula, M., Korpimäki, E., Siitari, H. and Viitala, J. (2002). Ultraviolet vision and foraging in terrestrial vertebrates. Oikos, 98, pp.505-511.
How, M., Zeil, J., & Hemmi, J. (2008). Variability of a dynamic visual signal: the fiddler crab claw-waving display. Journal of Comparative Physiology A, 195, pp.55-67.
How, M., Pignatelli, V., Temple, S., Marshall, N., & Hemmi, J. (2012). High e-vector acuity in the polarisation vision system of the fiddler crab Uca vomeris. The Journal Of Experimental Biology, 215, pp.2128-2134.
Jordão, J., Cronin, T., & Oliveira, R. (2007). Spectral sensitivity of four species of fiddler crabs (Uca pugnax, Uca pugilator, Uca vomeris and Uca tangeri) measured by in situ microspectrophotometry. Journal of Experimental Biology, 210, pp.447-453.
Laidre, M., & Johnstone, R. (2013). Animal signals. Current Biology, 23, pp.R829-R833.
Latruffe, C., McGregor, P., & Oliveira, R. (1999). Visual signalling and sexual selection in male fiddler crabs Uca tangeri. Marine Ecology Progress Series, 189, pp.233-240.
Layne, J., Land, M., & Zeil, J. (1997). Fiddler crabs use the visual horizon to distinguish predators from conspecifics: a review of the evidence. Journal of the Marine Biological Association of the United Kingdom, 77, pp.43-54.
Marshall, N, Jones, J., & Cronin, T. (1996). Behavioural evidence for colour vision in stomatopod crustaceans. Journal of Comparative Physiology A, 179, pp.473-481.
Marshall, J., & Oberwinkler, J. (1999). Ultraviolet vision: The colourful world of the mantis shrimp. Nature, 401, pp.873-874
Menzel, R., (1979). Spectral sensitivity and color vision in invertebrates. Comparative physiology and evolution of vision in invertebrates. Berlin, Heidelberg: Springer, pp.503-580
Oliveira, R., & Custódio, M. (1998). Claw size, waving display and female choice in the European fiddler crab, Uca tangeri. Ethology Ecology & Evolution, 10, pp.241-251.
Skelhorn, J., Holmes, G., & Rowe, C. (2016). Deimatic or aposematic?. Animal Behaviour, 113, pp.e1-e3.
Zeil, J., & Hemmi, J. (2005). The visual ecology of fiddler crabs. Journal Of Comparative Physiology A, 192, pp.1-25.
Zeil, J., Hemmi, J., & Backwell, P. (2006). Fiddler crabs. Current Biology, 16, pp.R40-R41.