Signals from crabworld: cuticular reflections in a fiddler crab colony
Centre for Visual Sciences, Research School of Biological Sciences, Australian National University, PO Box 475, Canberra ACT 2601, Australia
*Author for correspondence (e-mail: zeil{at}rsbs.anu.edu.au)
Accepted April 19, 2001
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Summary |
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Key words: Fiddler crab, Uca vomeris, specular reflection, polarization reflection, cuticle colour, colour change.
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Introduction |
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First, in mating and territorial interactions, males need to be able to detect either resident or wandering females, and males that are too close to their sphere of influence. Fiddler crabs are known to have two basic mating systems (Christy and Salmon, 1984; Christy and Salmon, 1991). In the first type, which is prevalent in our study animal, Uca vomeris, males need to detect resident females and to track them back to their burrows, where courtship and mating take place (Salmon, 1984). In the second principal mating system, receptive females wander through the colony and males need to attract them to their own burrows for mating. At present, we have no idea whether there is any pressure on males to maximise the distance at which they can detect females or discriminate them from males. In both mating systems, this will depend on the activity range of males, which in both situations is likely to be limited by constraints imposed by the homing system, which has been shown to rely exclusively on path integration (Zeil, 1998; Zeil and Layne, 2001). We are equally ignorant about what visual tasks female fiddler crabs are confronted with in the context of mating interactions. We do not know, for instance, to what degree females attract males by signalling in those mating systems in which courtship and mating occurs at the surface in the entrance of the female burrow. In the mating systems in which mating occurs underground in male burrows, wandering females do react to waving males and possibly choose by size and/or other cues which male to follow (Backwell and Passmore, 1996; Jennions and Backwell, 1996). It would seem that, in both mating systems, both males and females need to distinguish between the sexes, possibly by noting the presence or absence of an enlarged claw (von Hagen, 1962; von Hagen, 1970; Salmon and Stout, 1962; Land and Layne, 1995a).
A second context in which both male and female fiddler crabs need to be sensitive to the presence of other crabs is in burrow surveillance (Zeil and Layne, 2001). The burrow is a valuable resource for fiddler crabs and they have to worry continuously about defending it against burrow snatchers. Depending on their size, the crabs cease to see the entrance to their burrows after having moved away from it by approximately 1020cm during a foraging excursion, as corrective manoevres during homing and burrow closure experiments show (Zeil, 1998; Zeil and Layne, 2001). Burrow owners, nevertheless, are very sensitive to other crabs approaching their burrow even if their foraging excursions have led them away from home for quite large distances (possibly up to 1m). In response to other crabs approaching their (not visible) burrow, the crabs rush back to defend it. In this particular context there indeed appears to be pressure on maximising the distance at which other crabs can be detected, but not necessarily discriminated.
Third, fiddler crab colonies are dynamic societies. Burrow ownership is hotly contested and male crabs especially are repeatedly challenged by neighbours or immigrants and may lose the resulting contests. Crabs that have been evicted from their burrows or that have decided to leave their burrow for other reasons wander through the colony in search of a new home. Wandering crabs are more vulnerable to bird predation and are probably the main target for predatory birds (e.g. Ens et al., 1993; Land, 1999). Wanderers protect themselves by approaching burrow owners, which react by retreating to their burrows. Wanderers track retreating burrow owners back to their burrows and, despite being chased away, attach themselves to these foreign burrows by starting path integration at some point during the interaction when they have come sufficiently close to the foreign burrow. The rationale behind this behaviour is that, in moments of danger, both burrow owner and wanderer take cover in the same burrow (Zeil and Layne, 2001). As in burrow surveillance, there appears to be pressure on wandering crabs to maximise the distance at which they can detect burrow owners. It may also pay them to be able to judge whether another crab is relatively larger or smaller than themselves. Since burrow owners always try to chase a wanderer away, interactions with equally sized or smaller crabs may be safer, although approaching very much smaller crabs may also be dangerous because their narrow burrows do not offer protection.
What then, in the visual world of a fiddler crab, identifies another crab? On the most elementary level, the answer is: anything that moves in the ventral visual field and that has a minimum angular size of 24° (Land and Layne, 1995a). Although feeding crabs on the surface are slowly moving or still, they do produce a variety of motion signals by the movements of their feeding claws, by locomotion and by the waving displays of both males and females (e.g. von Hagen, 1993; Zeil and Zanker, 1997). Since motion detection relies on correlated changes in light intensity in neighbouring photoreceptors, a prerequisite for detecting image motion is the ability to detect differences in luminance. Image motion may not always allow a crab to distinguish conspecifics from other sympatric animal species, such as the much larger Macrophthalmus sp. crabs or mudskippers. Beside luminance contrast and motion patterns, colour and polarisation contrast may provide important cues for the presence of a conspecific crab. To explore these possibilities, we provide here a first survey of cuticular reflections as they occur in colonies of Uca vomeris and examine what relevance they may have both for intra-specific detection, monitoring and signalling and in the context of predation.
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Materials and methods |
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Video footage was recorded with a Sony DCR-TRV110E digital camcorder and a Hamamatsu ultraviolet-sensitive camera (Beam Finder III, C5332 series), the latter being equipped with a filter combination that passed ultraviolet from 300400nm only (Oriel No. 51720 and No. 51124). See Fig.3D for the spectral sensitivity of the camera, with and without filters. To determine, when required, the angular size of the camera image and to ensure that the cameras were placed at crab eye height, we filmed a vertical scale bar at a defined distance away from the camera that carried a marker at a defined height above the ground. The height of the camera was then adjusted such that the marker was aligned with the visual horizon line, indicating that the height of the camera lens corresponded exactly to the height of the marker.
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The raw data were stored on tape and resulted, after radiometrical calibration, in a series of single-waveband images with pixel values in units of µWs-1sr-1cm2nm-1. For most purposes, we transformed the images to units of photonsdegrees-2s-1nm-1. Downstream processing was performed using ENVI software, the IDL programming language (Research Systems, Colorado, USA) or Matlab (Mathworks, Natick, USA).
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Results |
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The signals
The most conspicuous signals we can identify in images taken from the viewpoint of a fiddler crab are the specular reflections returned by the smooth and wet cuticles of other crabs. The contrast of the signals generated by these specular reflections is enhanced by the fact that the ventral side of crabs is always in shadow and that the crabs themselves throw shadows onto the substratum. Viewed from the cockpit of a crab observer, other crabs appear as strong biphasic signals, with a dorsal component brighter than the background and a ventral component darker than the background (see transects on the right in Fig.2). Depending on the distance at which a crab is seen, these effects can become irrelevant to a crab observer as a result of the low-pass-filtering properties of the crab eye optics (compare left-hand transects in Fig.2).
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Since specular reflections are horizontally polarized, they are much more conspicuous when seen through a horizontal (Fig.4 left), than through a vertical (Fig.4 right) polarizer. The panels below the images in Fig.4 show the spectral reflectances of three selected points on the crabs cuticle (labelled 13) as measured through the horizontal (red) and the vertical (green) polarizer. The ratios of horizontal to vertical reflectances are given in the bottom panels (blue lines). Specular reflections can be distinguished from surfaces that are simply bright by virtue of the fact that they are polarized: the reflectance of the posterior surface of the males dactyl (the upper part of his enlarged claw) is virtually the same when measured through a horizontal or a vertical polarizer (grey and black lines in the centre panel in Fig.4; the locations of measurements are indicated by circles in the images). The degree of polarization reflection depends on the wetness of the surface, so that reflections are reduced in intensity when the cuticle is dry. As a consequence, crabs that have recently emerged from their burrows where they have had access to ground water, such as the crab on the right in the images shown in Fig.2, are much more conspicuous than crabs that have been operating on the surface for some time. Specular reflections are likely to be weaker when the sky is overcast. At the moment, we are not in the position to decide whether the fiddler crab cuticle itself has polarizing properties, as has been shown for some parts of the bodies of crayfish and mantis shrimps (Neville and Luke, 1971; Marshall et al., 1999).
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Discussion |
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The second property of their cuticle that fiddler crabs are able to control is the state of their chromophores, and with this the colour they present to an observer. There are several time scales over which these changes can occur. It has long been noted that the colours of crabs wax and wane following an endogenous rhythm that tracks the local tidal movements in their habitat (for reviews, see Thurman, 1988; Palmer, 1995). There are also indications that cuticle colours in fiddlers change depending on the mating status of crabs, on the level of stress and possibly on local diet (e.g. Crane, 1975; Wolfrath, 1993; Shih et al., 1999). We have shown here that, in Uca vomeris, these changes can occur within minutes (Fig.7), suggesting that they are subtle indicators of a crabs general state, but also that the crabs may be able to adjust their visibility to predatory birds or conspecifics.
The functional significance of these variable cuticle colours in fiddler crabs is largely unresolved, but must be influenced both by their role as intraspecific signalling and by the effect they have in making the crabs more detectable to predatory birds. Cuticle colours are likely to serve a multitude of functions, ranging from temperature control, through camouflage directed at predators and/or conspecifics, species recognition to intraspecific signalling for detectability, identity, status in the mating cycle, territorial status and, possibly, also for the state of fitness or quality. Despite the fact that fiddler crab colour changes have attracted scientific attention for over 100 years (for reviews, see Rao, 1985; Thurman, 1988), surprisingly little is known about their functional roles in the natural habitat and in the social life of these crabs (e.g. von Hagen, 1962; von Hagen, 1970; Crane, 1975; Wolfrath, 1993; Shih et al., 1999).
For Uca vomeris, it is striking to note that the colours differ depending on whether they are presented frontally or on the posterior part of the carapace: in the front, the colours are predominantly white and red, while on the back they are blue or white in the most colourful state an animal can reach (Fig.7). Compared with its appearance at long wavelengths, the mudflat is rather dark and homogeneous at short wavelengths, so that a blue signal will be quite conspicuous when seen by birds or by conspecifics against this background (Fig.7C). It will also predominantly stimulate a hypothetical short wavelength pigment of the crab eye (see below). The white colours that the crabs present with their claws and their display fronts will, in turn, be conspicuous across the human-visible spectrum and, thus, be stimulating short- and long-wavelength pigments to similar degrees. It may be significant that red colours dominate on those parts of the crabs that can be actively moved and are used in waving displays by both males and females (von Hagen, 1993): in U. vomeris at least, it is always the claws and the legs that are red, never the carapace (see Fig.5 for males and Fig.7 for females). Considering that in most animals the signals from only one receptor type, the green receptor, are fed into the motion-detection system, and that fiddler crabs may be dichromats (see below), this suggests that red colours and motion detection are linked, in the sense that they will exclusively stimulate only one of the two receptors.
The signals potentially available to a fiddler crab, as we have described them here, need at some stage be related to the spectral and polarization sensitivities of the crabs, which are at present unknown. Although we have a fair impression of the structure of the ommatidial sampling array in fiddler crabs (Zeil et al., 1986; Land and Layne, 1995a; Zeil and Al-Mutairi, 1996), we know little about their spectral and polarization sensitivities, let alone how they are distributed across the visual field. Electroretinograms (ERGs) suggest that fiddler crabs may possess only one pigment (Scott and Mote, 1974) with a peak sensitivity around 508nm, although Hyatt (Hyatt, 1975) has presented electrophysiological evidence (by selective adaptation of the ERG amplitude with ultraviolet and long-wavelength light) and behavioural evidence indicating that they may be dichromats with an additional short-wavelength pigment. Fiddler crabs do possess an 8th retinula cell (Uca coarctata; Sally Stowe, personal communication) which, in crayfish, has been shown to be a short-wavelength receptor (Cummins and Goldsmith, 1981). However, attempts to characterize the spectral sensitivities of fiddler crabs in more detail using microspectrophotometry have unfortunately failed (Cronin and Forward, 1988). Equally, there is behavioural evidence that fiddler crabs are polarization-sensitive (Altevogt and von Hagen, 1964; Korte, 1965), but the detailed structure of their rhabdoms, the degree to which their photoreceptors are polarization-sensitive and how this sensitivity is distributed across the visual field are not known.
At present we know too little about the physiology of their photoreceptors and the mechanisms of early visual processing in fiddler crabs to assess fully the significance of the specular reflections, polarization reflections and spectral reflections that their cuticle presents to a conspecific observer. In addition to characterizing spectral and polarization sensitivities, it will be important to determine the angular acceptance functions of receptor cells, to enable us to assess the absolute light sensitivity, the contrast sensitivity and, with this, the efficacy of these signals at the level of the retina. It will also be interesting to determine whether spectral and polarization sensitivities interact in fiddler crab eyes, as they do in butterflies (Kelber, 1999), and how adaptive this may be in processing the signals we have described here.
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Acknowledgments |
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References |
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Altevogt, R. (1959). Ökologische und ethologische Studien an Europas einziger Winkerkrabbe Uca tangeri Eydoux. Z. Morph. Ökol. Tiere 48, 123146.
Altevogt, R. and von Hagen, H.-O. (1964). Über die Orientierung von Uca tangeri Eydoux im Freiland. Z. Morphol. Ökol. Tiere 53, 636656.
Backwell, P. R. Y. and Passmore, N. I. (1996). Time constraints and multiple choice criteria in the sampling behaviour and mate choice of the fiddler crab, Uca annulipes. Behav. Ecol. Sociobiol. 38, 407416.
Chahl, J. S. and Srinivasan, M. V. (1997). Reflective surfaces for panoramic imaging. Appl. Opt. 36, 82758285.
Christy, J. H. (1995). Mimicry, mate choice and the sensory trap hypothesis. Am. Nat. 146, 171181.
Christy, J. H. and Salmon, M. (1984). Ecology and evolution of mating systems of fiddler crabs (Genus Uca). Biol. Rev. 59, 483509.
Christy, J. H. and Salmon, M. (1991). Comparative studies of reproductive behaviour in mantis shrimps and fiddler crabs. Am. Zool. 31, 329337.
Crane, J. (1975). Fiddler Crabs of the World. Princeton, NJ: Princeton University Press.
Cronin, T. W. and Forward, R. B. (1988). The visual pigments of crabs. I. Spectral characteristics. J. Comp. Physiol. A 162, 463478.
Cummins, D. and Goldsmith, T. H. (1981). Cellular identification of the violet receptor in the crayfish eye. J. Comp. Physiol. 142, 199202.
Ens, B. J., Klaassen, M. and Zwarts, L. (1993). Flocking and feeding in the fiddler crab (Uca tangeri): prey availability as risk-taking behaviour. Neth. J. Sea Res. 31, 477494.
George, R. W. and Jones, D. S. (1982). A Revision of the Fiddler Crabs of Australia. Records of the Western Australian Museum, Suppl. No. 14, 599.
Hyatt, G. (1975). Physiological and behavioural evidence for color discrimination by fiddler crabs (Brachyura, Ocypodidae, genus Uca). In Physiological Ecology of Estuarine Organisms (ed. V. Vernberg), pp. 333365. Columbia, SC: South Carolina University Press.
Jennions, M. D. and Backwell, P. R. Y. (1996). Residency and size affect fight duration and outcome in the fiddler crab Uca annulipes. Biol. J. Linn. Soc. 57, 293306.
Kelber, A. (1999). Why false colours are seen by butterflies. Nature 402, 251.[Medline]
Korte, R. (1965). Durch polarisiertes Licht hervorgerufene Optomotorik bei Uca tangeri. Experientia 21, 98.[Medline]
Kunze, P. (1963). Der Einfluss der Grösse bewegter Felder auf den optokinetischen Augennystagmus der Winkerkrabbe (Uca pugnax). Ergeb. Biol. 26, 5562.
Land, M. F. (1999). The roles of head movements in the search and capture strategy of a tern (Aves, Laridae). J. Comp. Physiol. A 184, 265272.
Land, M. F. and Layne, J. (1995a). The visual control of behaviour in fiddler crabs. I. Resolution, thresholds and the role of the horizon. J. Comp. Physiol. A 177, 8190.
Land, M. F. and Layne, J. (1995b). The visual control of behaviour in fiddler crabs: II. Tracking control systems in courtship and defence. J. Comp. Physiol. A 177, 91103.
Langdon, J. W. and Herrnkind, W. F. (1985). Visual shape discrimination in the fiddler crab, Uca pugilator. Mar. Behav. Physiol. 11, 315325.
Layne, J. E. (1998). Retinal location is the key to identifying predators in fiddler crabs (Uca pugilator). J. Exp. Biol. 201, 22532261.
Layne, J., Land, M. F. and Zeil, J. (1997). Fiddler crabs use the visual horizon to distinguish predators from conspecifics: A review of the evidence. J. Mar. Biol. 77, 4354.
Marshall, J., Cronin, T.W., Shashar, N. and Land, M. (1999). Behavioural evidence for polarisation vision in stomatopods reveals a potential channel for communication. Curr. Biol. 9, 755758.[Medline]
Nalbach, H.-O. and Nalbach, G. (1987). Distribution of optokinetic sensitivity over the eye of crabs: its relation to habitat and possible role in flow-field analysis. J. Comp. Physiol. A 160, 127135.
Neville, A. C. and Luke, B. M. (1971). Form optical activity in crustacean cuticle. J. Insect Physiol. 17, 519526.
Palmer, J. D. (1995). The Biological Rhythms and Clocks of Intertidal Animals. New York, Oxford: Oxford University Press.
Pelli, D. G. (1990). The quantum efficiency of vision. In Vision: Coding and Efficiency (ed. C. Blakemore), pp. 324. Cambridge: Cambridge University Press.
Rao, K. R. (1985). Pigmentary effectors. In The Biology of Crustacea, vol. 9 (ed. D. E. Bliss and L. H. Mantel), pp. 395462. New York, London: Academic Press.
Salmon, M. (1984). The courtship, aggression and mating system of a primitive fiddler crab (Uca vocans: Ocypodidae). Trans. Zool. Soc. Lond. 37, 150.
Salmon, M. and Stout J. F. (1962). Sexual discrimination and sound production in Uca pugilator Bosc. Zoologica 47, 1520.
Scott, S. and Mote, M. I. (1974). Spectral sensitivities in some marine Crustacea. Vision Res. 14, 659663.[Medline]
Shih, H.-T., Mok, H.-K., Chang, H.-W. and Lee, S.-C. (1999). Morphology of Uca formosensis Rathburn, 1921 (Crustacea: Decapoda: Ocypodidae), an endemic fiddler crab from Taiwan, with notes on its ecology. Zool. Stud. 38, 164177.
Thurman, C. L. (1988). Rhythmic physiological color change in crustacea: A review. Comp. Biochem. Physiol. 91C, 171185.
von Hagen, H.-O. (1962). Freilandstudien zur Sexual- und Fortpflanzungsbiologie von Uca tangeri in Andalusien. Z. Morph. Ökol. Tiere 51, 611725.
von Hagen, H.-O. (1968). Studien an peruanischen Winkerkrabben (Uca). Zool. Jb. Syst. 95, 395468.
von Hagen, H.-O. (1970). Die Balz von U. vocator (Herbst) als ökologisches Problem. Forma functio 2, 238253.
von Hagen, H.-O. (1993). Waving displays in females of Uca polita and of other Australian fiddler crabs. Ethology 93, 320.
Wolfrath, B. (1993). Observations on the behaviour of the European fiddler crab Uca tangeri. Mar. Ecol. Progr. Ser. 100, 111118.
Zeil, J. (1998). Homing in fiddler crabs (Uca lactea annulipes and Uca vomeris: Ocypodidae). J. Comp. Physiol. A 183, 367377.
Zeil, J. and Al-Mutairi, M. (1996). The variation of resolution and of ommatidial dimensions in the compound eyes of the fiddler crab Uca lactea annulipes (Ocypodidae, Brachyura, Decapoda). J. Exp. Biol. 199, 15691577.
Zeil, J. and Layne, J. E. (2001). Path integration in fiddler crabs and its relation to habitat and social life. In The Crustacean Nervous System (ed. K. Wiese). Heidelberg, Berlin New York: Springer Verlag (in press).
Zeil, J. and Zanker, J. M. (1997). A glimpse into crabworld. Vision Res. 37, 34173426.[Medline]
Zeil, J., Nalbach, G. and Nalbach H.-O. (1986). Eyes, eye stalks and the visual world of semi-terrestrial crabs. J. Comp. Physiol. A 159, 801811.
Zeil, J., Nalbach, G. and Nalbach H.-O. (1989). Spatial vision in a flat world: optical and neural adaptations in arthropods. In Neurobiology of Sensory Systems (ed. R. N. Singh and N. J. Strausfeld), pp. 123137. New York: Plenum Press.