Colouration and colour changes of the fiddler crab, Uca capricornis: a descriptive study

Colour changes in animals may be triggered by a variety of social and environmental factors and may occur over a matter of seconds or months. Crustaceans, like fiddler crabs (genus Uca), are particularly adept at changing their colour and have been the focus of numerous studies. However, few of these studies have attempted to quantitatively describe the individual variation in colour and pattern or their adaptive significance. This paper quantitatively describes the colour patterns of the fiddler crab Uca capricornis and their ability to change on a socially significant timescale. The most dramatic changes in colour pattern are associated with moulting. These ontogenetic changes result in a general reduction of the colour pattern with increasing size, although females are more colourful and variable than similarly-sized males. Uca capricornis are also capable of rapid colour changes in response to stress, but show no endogenous rhythms associated with the semilunar and tidal cycles commonly reported in other fiddler crabs. The extreme colour polymorphism and the relative stability of the colour patterns in Uca capricornis are consistent with their use in visually mediated mate recognition.     

Mate choice and the operational sex ratio: an experimental test with robotic crabs

The operational sex ratio (OSR: sexually active males: receptive females) predicts the intensity of competition for mates. It is less clear, however, under what circumstances, the OSR predicts the strength of sexual selection – that is, the extent to which variation in mating success is attributable to traits that increase the bearer's attractiveness and/or fighting ability. To establish causality, experiments that manipulate the OSR are required. Furthermore, if it is possible to control for any OSR‐dependent changes in the chosen sex (e.g. changes in male courtship), we can directly test whether the OSR affects the behaviour of the choosing sex (e.g. female choice decisions). We conducted female mate choice experiments in the field using robotic models of male fiddler crabs (Uca mjoebergi). We used a novel design with two females tested sequentially per trial. As in nature, the choice of the first female to mate therefore affected the mates available to the next female. In general, we detected significant sexual selection due to female choice for ‘males’ with larger claws. Importantly, the strength of sexual selection did not vary across five different OSR/density treatments. However, as the OSR decreased (hence the number of available males declined), females chose the ‘males’ with the largest claws available significantly more often than expected by chance. Possible reasons for this mismatch between the expected and observed effects of the OSR on the strength of sexual selection are discussed.     

Visually mediated species and neighbour recognition in fiddler crabs (Uca mjoebergi and Uca capricornis)

Mating signals are often directed at numerous senses and provide information about species identity, gender, receptiveness, individual identity and mate quality. Given the diversity of colourful body patterns in invertebrates, surprisingly few studies have examined the role of these visual signals in mate recognition. Here, we demonstrate the use of claw coloration as a species recognition signal in a fiddler crab (Uca mjoebergi). Furthermore, we show that distinct carapace colour patterns in Uca capricornis enable males to discriminate between their female neighbours and unfamiliar females. This is the first empirical evidence of the social importance of colour markings in fiddler crabs and the first example of visually mediated species and neighbour recognition in invertebrates other than insects.     

The effect of claw size and wave rate on female choice in a fiddler crab

How do females select a mate when they have mating preferences for multiple male traits? In experimental studies, female fiddler crabs (Uca mjoebergi) show a strong preference for males with larger claws and higher wave rates. In the field, there is no correlation between male claw size and observed wave rate. Here we document natural mating behaviour and show that females approach males who wave at a higher rate than nearby competitors. On average, an approached male had a significantly larger claw than his two nearest neighbours but did not differ in size from his two closest waving competitors. In general, smaller males were less likely to wave at approaching females. Females therefore approached mates based directly on wave rate but, because smaller males were less likely to wave, this indirectly resulted in female choice for larger than average males. Our study raises two issues. First, how do we relate the field results to previous experimental studies showing a female preference for larger claws? Second, in U. mjoebergi, males defend smaller neighbours against intruders. Our study suggests that one benefit of such defence coalitions is to decrease the number of immediate competitors present during female mate choice by retaining smaller neighbours.     

Sex, size and colour in a semi-terrestrial crab, Heloecius cordiformis (H. Milne Edwards, 1837)

We investigated the relationship between sex, size and colour in the little studied Australian endemic semaphore crab, Heloecius cordiformis, and related it to the crabs' social system with the aim of identifying the potential signalling function of claw colour.Equal sampling of crabs from all size classes revealed a strong relationship between sex, size and claw colour. Purple-clawed males were larger and had larger claws than pink-, orange- or green-clawed males. Male claws showed positive allometric growth: relative to body size, purple-clawed males had larger claws. The largest females had pink claws; the few with purple claws were no larger than immature green-clawed crabs. Female claws grow isometrically with the body so the relative claw size did not differ among the female colour classes. Quantitative measurements of claw colour revealed spectral differences between these subjectively described colours. The purple claws typical of large males also contrasted more strongly against the mudflat background than the other colours.Heloecius copulate outside female-owned burrows and probably within male-owned burrows. The male's waving display, in which both claws are raised and lowered, may feature in both mating strategies: as a territorial display and to attract wandering females. Large males are competitively superior so size, and potentially colour, are important in territorial disputes and may also feature in mate choice.     

Male mating success in a fiddler crab: a lesson in sample sizes

Autotomy and regrowth of a body part occurs in many animal species. It is costly to regrow the limb and there are often additional long-term costs in, for example, limb strength, foraging efficiency and even mating success. In the fiddler crab Uca mjoebergi, 7 % of males have autotomized and regrown their large claw at some point in their lives. Previous work has shown that there is a great disadvantage to having a regenerated claw. While these males are able to attract mate-searching females to visit them, none of the 84 males observed to have mated in previously collected data had regenerated claws. Since females’ final mate choice is based on burrow structure, it was assumed that males with regenerated claws had poorer burrows. Here we show that, by finding only three cases of a female mating with a regenerated claw male, that there is, in fact, no mating disadvantage to having a regenerated claw. We also show that the burrows of males with regenerated claws are no different than those of orginal-clawed males. This is a very clear reminder that sample size matters, especially when dealing with rare events.     

Dishonest signalling in a fiddler crab

Animal communication theory predicts that low-frequency cheating should be common in generally honest signalling systems. However, perhaps because cheats are designed to go undetected, there are few examples of dishonest signals in natural populations. Here we present what we believe is the first example of a dishonest signal which is used commonly by males to attract mates and fight sexual rivals. After losing their large claw male fiddler crabs (Uca annulipes) grow a new one which has less mass, is a less effective weapon and costs less to use in signalling than an equivalent-length claw of the original form. Males with original claws do not differentially fight males with regenerated claws even though they are likely to win. Regenerated claws effectively bluff fighting ability and deter potential opponents before they fight. During mate searching, females do not discriminate against males with low-mass, regenerated claws, indicating that they are deceived as to the true costs males pay to produce sexual signals. Up to 44% of males in natural populations have regenerated claws, a level unanticipated by current signalling theory. The apparent rarity of cheating may be an artefact of the usual difficulty of detecting cheats and dishonesty may be quite common.     

Air pollution fades the plumage of the Great Tit

1. Great Tits ( Parus major ) derive the carotenoid pigments for their yellow plumage via the prey items in their diet. Air pollution is known to affect the abundance of many forest insects, e.g. green caterpillars, which are an important source of food and pigments for tits. This study investigates whether air pollutants indirectly affected the intensity of the yellow colour in P. major plumage via the reduced access to carotenoid sources.
2. The intensity of the yellow colour in the plumage of P. major nestlings was scored and the relative abundance of green herbivorous larvae in territories around a polluting copper smelter in SW Finland was simultaneously measured.
3. Both the intensity of yellow colour in nestling plumage and caterpillar abundance increased with increasing distance from the pollution source. The colour intensity correlated significantly with the density of green herbivorous larvae in a territory.
4. Parus major nestlings were significantly heavier at distant sites than close to the pollution source which suggests that the future survival probability of pale nestlings may be lowered.
5. Young birds, after their first moult, were studied for the relationships between condition, size and plumage colour by the means of ptilochronology. The plumage colour intensity did not correlate with the size corrected width of the growth bars in fifth rectrix (condition at moult) but was correlated positively with the length of the rectrix (size).
6. The implications of colour change for survival and mate choice are discussed.     

The relative role of male vs. female mate choice in maintaining assortative pairing among discrete colour morphs

Mate choice has important evolutionary consequences because it influences assortative mating and the level of genetic variation maintained within populations. In species with genetically determined polymorphisms, nonrandom mate choice may affect the evolutionary stability and maintenance (or loss) of alternative phenotypes. We examined the mating pattern in the colour polymorphic Gouldian finch (Erythrura gouldiae), and the role of mate choice, both female and male, in maintaining the three discrete head colours (black, red and yellow). In both large captive and wild populations, Gouldian finches paired assortatively with respect to head colour. In mate choice trials, females showed a strong preference for mates with the most elaborate sexually dimorphic traits (i.e. more chromatic UV/blue plumage and longer pin-tail feathers), but did not discriminate assortatively. Unexpectedly, however, males were particularly choosy, associating and pairing only with females of their own morph-type. Although female mate choice is generally invoked as the major selective force maintaining conspicuous male colouration in sexually dichromatic species, and is typically thought to drive nonrandom mating, these findings suggest that mutual mate choice and male mate choice in particular, are an important yet neglected component of selection.     

Sexual selection and non-random mating for shell colour in a natural population of the marine snailLittorina mariae (Gastropoda: Prosobranchia)

In order to estimate the three independent components of mating behaviour, sexual selection in females, sexual selection in males and mating pattern, we studied the distribution of shell colour morphs among mating pairs and between copulating and non-copulating snails in four subsamples of a natural population ofL. mariae. The colour of the shell, the sex and a qualitative estimate of age was recorded for every snail. We found sexual selection acting against one of the two commonest colours (yellow) among the young females. However, in males none of the eight shell colour morphs was favoured during matings. Male sexual choice or differences in female sexual activity may cause the sexual fitness disadvantage of yellow females. Moreover, individuals of different colour morphs did not mate at random, rather dissasortatively. A behavioural choice among shell colour morphs or a non-random microdistribution of the morphs may cause the departure from random mating in this population.     

Ultraviolet reflection and female mate choice in the pied flycatcher, Ficedula hypoleuca

In pied flycatchers females seem to prefer male territory quality rather than male characteristics, and the results of female mate choice experiments are divergent. In this outdoor aviary study, we examined how altering the ultraviolet reflection of males affects female mate choice behaviour. We chose pairs of males with similar human-visible dorsal colour and morphological traits. We then reduced the proportional ultraviolet reflectance in one male with sunscreen chemicals. The other male was treated with a chemical that slightly increased the ultraviolet reflectance of the plumage. In the experiment females clearly preferred males with slightly increased ultraviolet reflection. Our results indicate that pied flycatcher females use ultraviolet cues for mate choice when the effect of territory quality is controlled for. The results give us new information about a possible mechanism of mate assessment in this species, and indicate the importance of colour cues in avian mate choice behaviour.     

Sexual selection and the physiological consequences of habitat choice by a fiddler crab

In mid-Atlantic salt marshes, reproductively active male sand fiddler crabs, Uca pugilator, use a single greatly enlarged major claw as both a weapon to defend specialized breeding burrows from other males and an ornament to attract females for mating. During the summer breeding season, females strongly prefer to mate with males controlling burrows in open areas high on the shore. Food availability decreases while temperature and desiccation stress increase with increasing shore height, suggesting that the timing and location of fiddler crab mating activity may result in a potential trade-off between reproductive success and physiological condition for male crabs. We compared thermal preferences in laboratory choice experiments to body temperatures of models and living crabs in the field and found that from the perspective of a fiddler crab, the thermal environment of the mating area is quite harsh relative to other marsh microhabitats. High temperatures significantly constrained fiddler crab activity on the marsh surface, a disadvantage heightened by strongly reduced food availability in the breeding area. Nevertheless, when the chance of successfully acquiring a mate was high, males accepted a higher body temperature (and concomitantly higher metabolic and water loss rates) than when the chances of mating were low. Likewise, experimentally lowering costs by adding food and reducing thermal stress in situ increased fiddler crab waving display levels significantly. Our data suggest that fiddler crabs can mitigate potential life history trade-offs by tuning their behavior in response to the magnitude of both energetic and non-energetic costs and benefits.     

Beauty in the eyes of the beholders: colour vision is tuned to mate preference in the Trinidadian guppy (Poecilia reticulata)

A broad range of animals use visual signals to assess potential mates, and the theory of sensory exploitation suggests variation in visual systems drives mate preference variation due to sensory bias. Trinidadian guppies (Poecilia reticulata), a classic system for studies of the evolution of female mate choice, provide a unique opportunity to test this theory by looking for covariation in visual tuning, light environment and mate preferences. Female preference co‐evolves with male coloration, such that guppy females from ‘low‐predation’ environments have stronger preferences for males with more orange/red coloration than do females from ‘high‐predation’ environments. Here, we show that colour vision also varies across populations, with ‘low’‐predation guppies investing more of their colour vision to detect red/orange coloration. In independently colonized watersheds, guppies expressed higher levels of both LWS‐1 and LWS‐3 (the most abundant LWS opsins) in ‘low‐predation’ populations than ‘high‐predation’ populations at a time that corresponds to differences in cone cell abundance. We also observed that the frequency of a coding polymorphism differed between high‐ and low‐predation populations. Together, this shows that the variation underlying preference could be explained by simple changes in expression and coding of opsins, providing important candidate genes to investigate the genetic basis of female preference variation in this model system.     

Ontogenetic colour change signals sexual maturity in a non-territorial damselfly

Conspicuous colouration increases male reproductive success through female preferences and/or male–male competition. Despite the advantages of conspicuous colouration, inconspicuous male morphs can exist simultaneously in a population due to genetic diversity, condition dependence or developmental constraints. We are interested in explaining the male dichromatism in Xanthagrion erythroneurum damselflies. We reared these damselflies in outdoor insectaries under natural conditions and showed that this species undergoes ontogenetic colour changes. The younger males are yellow and change colour to red 6–7 days after their emergence. We took red and yellow male reflectance spectra and found that red males are brighter than yellow males. Next, we aimed to determine whether ontogenetic colour change signals sexual maturity with field observations and laboratory experiments. Our field observational data showed that red males are in higher abundance in the breeding territory, and they have a higher mating frequency than yellow males. We confirmed these field observations by enclosing a red and a yellow male with two females and found that yellow males do not mate in presence of red males. To determine whether colour change signals sexual maturity, we measured mating success of males before and after colour changes by enclosing a single male at different age (day 3-day 7) and colour (yellow, intermediate and red) with a single female in a mating cage. Males did not mate when yellow but the same male mated after it changed colour to red, suggesting the ontogenetic colour change signals sexual maturity in this species. Our study shows that male dichromatism can be age-dependent and ontogenetic colour change can signal age and sexual readiness in non-territorial insects.     

Heritability and heterochrony of polychromatism in a Lake Victoria Cichlid fish: Stepping stones for speciation?

In many haplochromine cichlid fish, male nuptial coloration is subject to female mate choice and plays a central role in the evolution of reproductive isolation between incipient species. Intraspecific variation in male coloration may serve as a target for diversifying sexual selection and provide a starting point for species divergence. Here, we investigated a polychromatism in Neochromis omnicaeruleus, a haplochromine from Lake Victoria, East-Africa. In this species, male coloration ranges from skyblue to yellow-red and females are grey-blue to yellow. We found that both genetic and environmental factors influence the expression of these colours during individual development. In a natural population, we found that male colour was associated with size and sexual maturity: yellow males were smaller than blue males and tended to be sexually immature. In females, size and maturity did not differ between colour types. Laboratory crosses revealed that there is a heritable component to the observed colour variation: yellow parents produced more yellow offspring than blue parents. Together with repeated aquarium observations of yellow individuals that gradually become blue, these data suggest that yellow males change to blue as they approach sexual maturity, and that the occurrence and timing of this transition is influenced by both environmental and genetic effects. The significance of this mechanism of colour expression as a possible target for divergent selection remains to be evaluated.     

Regulation of sex-specific feeding behavior in fiddler crabs: physiological properties of chemoreceptor neurons in claws and legs of males and females

This study examined properties of chemoreceptor neurons in the claws and legs of the fiddler crabs Uca pugilator and U. pugnax. The primary goal was to establish the neural basis of previously observed greater female sensitivity to feeding stimulants, and secondarily to compare physiological properties of chemoreceptor neurons in these semi-terrestrial crustaceans with those of fully aquatic forms. Sensitivity of chemoreceptor neurons in claws and legs is sex-specific; individual neurons of females respond to lower stimulus concentrations than male chemoreceptor neurons, and equivalent concentrations elicit greater spiking in female vs male chemoreceptor neurons. Thus, the population of chemoreceptor neurons in females expresses lower thresholds and greater average sensitivity than in males. Greater sensitivity of claw neurons explains observations indicating that females continue to feed at food levels too low to stimulate males. Sensitivity differences in leg neurons of males vs females have no clear behavioral correlate, but suggest that females can orient to more dilute stimuli than males. Chemoreceptor neurons of fiddler crabs have low sensitivities and slow rates of adaptation compared to other crustaceans. Also, neurons in claws adapt less slowly than neurons in legs, which may reflect subtle differences in the chemical stimulus environment experienced by claws vs legs.     

Ultraviolet colour vision and ornamentation in bluethroats

Many birds see in the ultraviolet (300–400 nm), but there is limited evidence for colour communication (signalling by spectral shape independently of brightness) in this ''hidden'' waveband. Such data are critical for the understanding of extravagant plumage colours, some of which show considerable UV reflectance. We investigated UV colour vision in female social responses to the male UV/violet ornament in bluethroats, Luscinia s. svecica. In an outdoor aviary at the breeding grounds, 16 females were each presented with a unique pair of males of equal age. In UVR (UV reduction) males, sunblock chemicals reduced only the UV reflectance and thereby the spectral shape (colour) of the throat ornament. In NR (neutral reduction) males, an achromatic pigment in the same base solvent (preen gland fat) was used for a corresponding but uniform brightness reduction. Both colour and brightness effects were invisible to human eyes, and were monitored by spectrometry. In 13 of the 16 trials, the female associated most with the NR male, a preference that implies that UV colour vision is used in mate choice by female bluethroats. Reflectance differences between one-year-old and older males were significant only in UV, suggestive of a UV colour cue in age-related mate preferences.     

Mate choice and the genetic basis for colour variation in a polymorphic dart frog: inferences from a wild pedigree

Understanding how reproductive barriers evolve during speciation remains an important question in evolution. Divergence in mating preferences may be a common first step in this process. The striking colour pattern diversity of strawberry dart frog (Dendrobates pumilio) populations has likely been shaped by sexual selection. Previous laboratory studies have shown that females attend to male coloration and prefer to court with males of their own colour, suggesting that divergent morphs may be reproductively isolated. To test this hypothesis, we used molecular data to estimate pedigree relationships from a polymorphic population. Whereas in the laboratory both red and yellow females preferred to court with males of their own phenotype, our pedigree shows a pattern of assortative mating only for red females. In the wild, yellow females appear to be less choosy about their mates, perhaps because they incur higher costs associated with searching than females of the more common red phenotype. We also used our pedigree to investigate the genetic basis for colour-pattern variation. The phenotype frequencies we observed were consistent with those expected if dorsal background coloration is controlled by a single locus, with complete dominance of red over yellow. Our results not only help clarify the role of sexual selection in reducing gene flow, but also shed light on the mechanisms underlying colour-pattern variation among sympatric colour morphs. The difference we observed between mating preferences measured under laboratory conditions and the pattern of mate choice observed in the wild highlight the importance of field studies for understanding behavioural reproductive isolation.     

Ultra-violet reflectance of male and female red grouse, Lagopus lagopus scoticus, sexual ornaments reflect nematode parasite intensity

In many birds, females prefer males with the biggest or brightest sexual ornaments, which might reflect a higher phenotypic quality, such as fewer parasites. Unlike humans, most birds detect near-ultraviolet (UV) light, and UV signals can play an important role in sexual signalling and mate choice. Using a spectrophotometer, we analysed the colour of red grouse Lagopus lagopus scoticus sexual ornaments (their combs). We first show that combs reflect both in the red (600–700 nm) and UV (300–400 nm) part of the spectrum. Second, we investigated whether comb size and colour, and UV reflectance in particular, reflected an aspect of individual quality: the intensity of infection by a main nematode parasite, the caecal threadworm Trichostrongylus tenuis . We first analysed comb size and colour variation, and parasite intensity variation, in relation to sex and age. Males had bigger and redder combs than females, but UV brightness was greater for female than for male combs. Comb colour also differed between age groups, with young birds of both sexes showing brighter UV than old birds. Young grouse also had fewer T. tenuis worms than old grouse. We further tested whether intensity of infection could be predicted from comb characteristics (size and colour) in male and female red grouse. We found that parasite intensity was not significantly related to comb size or red brightness, but fewer worms were predicted from brighter UV in combs, in both males and females. The results indicate that UV reflectance of combs have a quality revealing function and might play an important role in grouse mate choice: UV brightness of combs could enable both male and female red grouse to assess the parasite loads of a potential mate.     

Carotenoid-based bill colour as an indicator of immunocompetence and sperm performance in male mallards

Female mate choice is often based on exaggerated sexual traits, signals of male qualities that females cannot assess directly. Two such key qualities are male immune and/or sexual competence, whereby honesty in signalling could be maintained by physiological trade-offs. Carotenoid-based ornaments likely constitute such honest signals, as there is direct competition for (limited) carotenoids between ornament deposition and anti-oxidant support of immune or sperm functioning. Using spectrometry, we assessed the potential signalling function of the yellow, carotenoid-based colour of the bill of male mallards, a target of female mate choice. Here we demonstrate that bill reflectance varied with plasma carotenoid level, indicating antioxidant reserves. Moreover, lower relative UV reflectance during autumn pairing predicted immune responsiveness and correlated positively with sperm velocity during breeding, a trait that affects fertility. Our data provide support for current theories that females could use carotenoid-based sexual signals to detect immune vigour and fertilizing ability of prospective mates.