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.     

Sex, sensitivity, and second messengers: differential effect of cyclic nucleotide mediated inhibition in the chemosensory system of fiddler crabs

Fiddler crabs (Uca spp.) exhibit sex-specific responses food-related chemical cues, constituting a natural experiment regarding the regulation of chemosensitivity. To understand the mechanisms that underlie these broad differences, chemosensory neurons from the claws were challenged with stimulants in the presence of various agents that activate or inhibit the adenylate cyclase-cAMP transduction cascade. Stimulants mixed with agents that increase intracellular cAMP (forskolin, 3-isobutyl-1-methylxanthine, and Ro 20-1724) elicited decreased response magnitudes from neurons, compared to drug-free controls, whereas the adenylate cyclase inhibitor SQ 22536 increased the response. These effects were dose dependent and reversible, and, in all cases, were more dramatic in male than in female neurons. Similar to other crustaceans, the adenylate cyclase-cAMP second-messenger system appears to regulate inhibition in fiddler crab chemosensory neurons. The perturbations of this pathway reveal that the degree of inhibition is greater in male than in female neurons, consistent with the lower behavioral and physiological sensitivity typically displayed by males. Changes in the expression of the second messenger system may be causal in the production of sex-specific patterns of chemosensitivity that underlie behavior. Alternately, experimental perturbations using adenylate cyclase-cAMP pathway modulators may unmask sex-specific differences in electrical properties of peripheral neurons affecting action potential generation.     

Visual and Acoustical Signalling during Courtship by Fiddler Crabs (Genus Uca)

Male fiddler crabs (Genus Uca) employ both visual and acousticalsignals to attract females for mating. In U. pugilator and severalother American species, the males attract females during theday first by waving, then by producing sounds just within theirburrows. At night, the males produce sounds at low rates, butwhen touched by a female, they increase their rate of soundproduction. In the European species, U. tangeri, many elements of courtshipare similar to those in U. pugilator, but two types of soundsare produced. One of these, the short drumwhirl, appears tosubstitute for waving when the male is temporarily obscuredfrom the female during his diurnal courtship activities. Thelong drumwhirl is used under different circumstances. The acoustical responses of a male to a female influence thecourtship behavior of other males in the area. When sounds fromstimulated males are played back to test males during the day,their lates of waving increase. At night, the playbacks elicitincreases in rates of sound production. The influence of tidal oscillations, temperature, and lightcycles on the behavior of males is discussed. Courtship activities of aquatic crabs are compared to thoseof terrestrial Brachyura. In aquatic forms, courtship may beabsent or, if present, does not involve elaborate signallingby the male. Chemical or visual cues at close range are themost important stimuli. In several genera of terrestrial crabs,visual signalling for prolonged periods is common, and soundsare often emitted by males to "call" females from their burrowsto the surface for mating. Some of the factors that may accountfor differences in courtship activities in aquatic and terrestrialspecies are discussed.     

Semi-monthly reproductive cycles in male and female fiddler crabs, Uca pugnax

In the fiddler crab, Uca pugnax, numbers of displaying males, numbers of burrows with half-dome superstructures (hoods), numbers of females with decalcified vulvar opercula, and numbers of females hatching their eggs, all follow a semi-monthly cycle with peaks near the time of the spring tides. These are all aspects of reproduction in Uca. Decalcification of female opercula, although necessary for mating and egg deposition, is neither necessary nor sufficient for behavioural response to courting males. In fact, behavioural responsiveness to males probably precedes decalcification in most cases. The different aspects of the reproductive cycle are coordinated so that females and males are ready to mate at about the same time near one spring tide, and the resulting eggs will be ready to hatch on the next spring tide. Two decalcified females which were kept isolated from males produced fertile clutches, suggesting that stored sperm from a previous mating may fertilize eggs in a later cycle. This may be one reason for the relative rarity of observed matings or precopulatory behaviour in Uca.     

A Spatially Explicit Model of Synchronization in Fiddler Crab Waving Displays

Fiddler crabs (Uca spp., Decapoda: Ocypodidae) are commonly found forming large aggregations in intertidal zones, where they perform rhythmic waving displays with their greatly enlarged claws. While performing these displays, fiddler crabs often synchronize their behavior with neighboring males, forming the only known synchronized visual courtship displays involving reflected light and moving body parts. Despite being one of the most conspicuous aspects of fiddler crab behavior, little is known about the mechanisms underlying synchronization of male displays. In this study we develop a spatially explicit model of fiddler crab waving displays using coupled logistic map equations. We explored two alternative models in which males either direct their attention at random angles or preferentially toward neighbors. Our results indicate that synchronization is possible over a fairly large region of parameter space. Moreover, our model was capable of generating local synchronization neighborhoods, as commonly observed in fiddler crabs under natural conditions.     

Behavioral and electrophysiological experiments suggest that the antennular outer flagellum is the site of pheromone reception in the male helmet crab Telmessus cheiragonus

Sexually competent females of Telmessus cheiragonus (helmet crab) release two pheromones that elicit grasping and copulation behaviors in males (Kamio et al., 2000, 2002, 2003). Our study aimed to use behavioral and electrophysiological techniques to identify the site of reception of these sex pheromones. In behavioral experiments, either the inner or the outer flagella of the antennules were ablated bilaterally from male crabs, and responses of male crabs to female odor were examined. When the inner flagella were surgically ablated, the sexual response (i.e., grasping and copulation behavior) of male crabs was not significantly changed relative to control animals that had their second antennae ablated. In contrast, the sexual response was significantly reduced when the outer flagella of the antennules were ablated, suggesting that the outer flagellum is the receptor organ that detects the sex pheromones. In electrophysiological experiments, urine, which in females contains the pheromone that elicits grasping behavior by males but does not contain the pheromone eliciting copulation, whose release site is not known, was tested. Female and male urine as well as shrimp extract evoked phasic responses of chemosensory afferents innervating aesthetasc sensilla on the outer flagellum of male crabs. The response of the afferents had significantly higher magnitude and lower threshold when female urine was applied. Thus, behavioral and electrophysiological observations suggest that in male helmet crabs, the outer flagellum of the antennule is the chemosensory organ that detects female sex pheromone.     

Distastefulness as a defense mechanism in Aplysia brasiliana (Mollusca: Gastropoda)

An unusual courtship pattern for fiddler crabs is described from field observations in Panama. This behavior pattern, referred to here as “directing,” differs considerably from the more frequently observed communal courtship system found in close relatives of Uca deichmanni. A male involved in “directing” approaches a female and attempts to carry or maneuver her into his burrow for mating. The female usually struggles to escape from the male. This activity often attracts other males which attempt to “direct” the female if she escapes from the first male. A male is most successful in “directing” a female into his burrow if a) he is larger than the female, b) the female is wandering (a sign of physiological receptivity) prior to the “directing” attempt, and c) several males attempt to “direct” the female at once. The results suggest that females are choosing mates by inciting several males to compete for them. The males which successfully “direct” the struggling females are probably the most fit males.     

Sex-specific mediation of foraging in the shore crab, Carcinus maenas

Experiments were conducted to investigate the sex-specific differences to feeding responses of the shore crab Carcinus maenas throughout the year. Results demonstrate that female shore crabs exhibit stronger feeding responses than males throughout the year with a significantly reduced feeding response in males during the summer months' reproductive season. We also studied the possible function(s) of the moulting hormone, 20-hydroxyecdysone (Crustecdysone) that has been described as a potential female-produced sex pheromone to initiate male reproductive behaviour in a number of crustaceans. We recently presented evidence that for shore crabs this is not the case and now show that the steroid is instead functioning as a sex-specific feeding deterrent protecting the moulting 'soft' female crabs. Whilst male shore crabs were deterred from prey (Mytilus edulis) and synthetic feeding stimulants glycine and taurine when these feeding stimulants were spiked with crustecdysone, intermoult female crabs were significantly less affected and rarely deterred from feeding. This sex specificity of the moulting hormone, in combination with the female sex pheromone, which has no anti-feeding properties, ensures that male crabs mate with soft-shelled, moulted females rather than engage in cannibalism, such as found frequently in cases when soft-shelled females are exposed to intermoult females.     

Eavesdropping in crabs: an agency for lady detection

Although conspicuous courtship displays are an effective way of attracting the attention of receptive females, they could provide valuable information to rival males on the location of these females. In fiddler crabs, males that see a receptive female wave their single, greatly enlarged claw in a highly conspicuous courtship display. We test whether other males use this courtship display to alert them to the presence of receptive females that they cannot directly see. We show that male fiddler crabs (Uca mjoebergi) eavesdrop on the courtship displays of nearby males to detect mate-searching females. This allows males to begin waving before a female becomes visible. Furthermore, males appear to adjust their waving according to the information available: eavesdropping males wave 12 times faster than non-courting males but only 1.7 times slower than males in full visual contact with the female.     

Comparative Studies of Reproductive Behavior in Mantis Shrimps and Fiddler Crabs

Comparative ethological studies of closely related species canplace into clear perspective the functions of behavioral traitsas species diverge and adapt to different environments. In thispaper we contrast the reproductive behavior of species withintwo crustacean groups: the mantis shrimps (stomatopods) andthe fiddler crabs (genus Uca). For the stomatopods, we identifyprobable selective relationships between features of species'ecology and their mating systems. Population density, the kindand availability of shelters in which these shrimps live, theintensity of predation and spawning cycles all play importantroles in molding reproductive behavior in this group. Associationsbetween the ecology and mating systems of fiddler crabs havebeen discussed recently elsewhere. Here we focus on a comparativeanalysis of sexual communication in these crabs. A study ofcompetitive courtship signaling and mate choice in the fiddlercrab Uca beebei has shown that certain male courtship signalsare highly attractive probably because they exploit female sensory-responsesystems that have been molded by selection for escape from predators.Interspecific comparison of male courtship displays and theresponses of females to these displays suggest that sensoryexploitation may play an important role in the evolution ofsexual signals in the genus. Comparative studies have advancedour understanding of how natural and sexual selection affectthe reproductive behavior of both stomatopods and fiddler crabs.     

Size-dependent mating preference of the male fiddler crab Austruca perplexa

In many animals, females prefer large males to small males, which allow large males to be choosier than small males when selecting a mate. We investigated the courtship intensity of small- and large-sized male fiddler crabs (Austruca perplexa) by examining their claw-waving rates (waves/min) towards small- and large-sized females. We found that large males showed a greater preference for large females by producing more waves/min towards them, whereas small males did not show any apparent preference for either large or small females. Moreover, the waving rate of large males was positively correlated with female size, but there was no correlation between waving rate and female size in small males. These results indicate that large males in a population become choosier and show strong mate choice, which is most likely due to their greater preference among females.     

Bilateral linkage of monomorphic and dimorphic limb sizes in fiddler crabs

In this study, the subject of whether investment in one bilateral structure was linked to investment in the homologous bilateral opposite structure was investigated. Male fiddler crabs (genus Uca, family Ocypodidae) displayed strong bilateral claw differentiation of function and size, which are used for feeding (minor claw) or display/combat (major claw). Females had similar‐sized feeding claws. Linkage between claw size was investigated by estimating the deviations from an overall fitted regression of claw length to body size. The positive correlations of the deviations of claw size for major and minor claws of males and between right and left claws of females, relative to body size, suggested a linkage in investment between one claw and the corresponding claw on the other side of the body, for both monomorphic females and dimorphic males. A signal to send resources may be effectively gated to the claw complex, suggesting that positively correlated resources are allocated to both claws. Positive correlations were also found at the interspecific level. The fiddler crab model, described here, gives access to study the linkage in symmetric and asymmetric bilateral structures in the same species with a connection to the macroevolutionary level.     

Behavioural evidence for body colour signaling in the fiddler crab Uca perplexa (Brachyura: Ocypodidae)

In the reproductive season, mature females of the fiddler crab Uca perplexa leave their burrows and wander about their habitat for mating. To clarify whether the fiddler crabs respond to colour or luminosity, I examined the behavioural responses of the males to the wandering females before and after the females were painted white, red, black or blue. The behaviours of the males were categorized into three types: lateral–circular wave and lateral–straight wave for courting, and repelling. Before painting, almost all of the males courted the females. After painting, significantly fewer males courted the red-, black- and blue-painted females than courted the white-painted females. These results mean that the fiddler crabs can discriminate colours or luminosity. The role of body colour as a visual signal in crab society is discussed.     

Stimulation of feeding behavior in three species of fiddler crabs by hexose sugars

Feeding responses to five hexoses were examined in three closelyrelated species of fiddler crabs, Uca minax, U.pugnax and U.pugilator.Hexoses tested were glucose, galactose, sorbose, fructose andmannose. Intact crabs and eyestalk-ablated crabs were tested.Responses to sugars were species specific. Eyestalks are directlyinvolved in vision and overall neural integration as well aswith chemosensory and metabolic pathways associated with feeding.Overall, eyestalk-ablated crabs were more sensitive uian intactcrabs. Studies of responses of individuals within a populationto hexoses showed tiiere are individual U.pugnax that respondto galactose and others that do not. Similarly, there were U.pugilatorindividuals that were mannose responsive and others that didnot respond to mannose. An additional study of differences inpopulation responses to hexoses would provide valuable toolsin studying geographic relationships between fiddler crab populations.     

Semilunar courtship rhythm of the fiddler crab<Emphasis Type="Italic"> Uca lactea</Emphasis> in a habitat with great tidal variation

Semilunar courtship rhythm is a widely distributed phenomenon among fiddler crabs in the genus Uca (Decapoda, Ocypodidae). Typically, synchronous courtship has been reported to peak near spring tides. To determine whether a region of large tidal variation shifts reproductive activity, we measured the frequency of specific courtship behaviors including claw-waving and semidome building for U. lactea males on Kanghwa Island, Korea. We found that synchronized courtship for U. lactea peaked near neap tides, whereas near the spring tides, seawater flooded the habitat and males predominantly fed on the mudflat. Although active females, which hold their burrows and usually feed on the mudflat, are abundant near to spring tides, males rarely claw-waved to attract females. This pattern is atypical for the species because other populations of U. lactea on Japan and Taiwan are synchronous around spring tides. We suggest that males invest most of their time in feeding during spring tides because foraging is limited during neap tides. During neap tides, males feed infrequently and thus expend stored energy on courtship signals. We conclude that patterns of reproductive synchrony may be dependent on food availability in periodically changing environments.     

Factors Affecting Mating Tactics in the Fiddler Crab, Uca vocans hesperiae

The mating strategies of male fiddler crabs are variable and highly flexible within species. In this study I examine three types of mating strategy used by individual male Uca vocans hesperaie. The most common strategy, termed a ‘standard gambit’, where males approached females at their burrow entrance and initiated courtship, accounted for 63% of mating attempts and 75% of successful matings. The rarest strategy (4% of mating attempts) was the ‘dig out’, where males attempted to mate with females whose burrows they had excavated. This strategy accounted for 19% of successful matings. ‘Herding’ behaviour which involved a male attempting to herd a female into a burrow and mate, contributed 33% of mating attempts but were generally unsuccessful, accounting for only 2.6% of successful matings. Males used more than one strategy during the study period. Smaller males used the standard gambit strategy more often than herding or dig outs while larger males used the herding strategy more often. There was no relationship between male size and mating success and males did not preferentially mate with females of a certain size. The predominant strategy adopted by males over the lunar cycle depended on female behaviour. Herding behaviour was induced by female wandering which escalated at full moon. Standard gambits were the commonest strategy adopted at and around new moon. The low success rate of male mating attempts (16%) indicates a reluctance by females to mate multiply. This may lead to conflict between the sexes because in fiddler crabs there is last male sperm precedence.     

Density affects mating mode and large male mating advantage in a fiddler crab

Fiddler crabs show two different mating modes: either females search and crabs mate underground in male burrows, or males search and crabs mate on the surface near female burrows. We explored the relationship between crab density, body size, the searching behavior of both sexes, and the occurrence of both mating modes in the fiddler crab Uca uruguayensis. We found that crabs change their mating mode depending on their size and crab density. Crabs mated mostly on the surface at low densities, and underground at high densities. The proportion of wandering receptive females but not courting males accounted for the variation in mating modes. This suggests that whether crabs mate underground (or on the surface) is determined by the presence (or absence) of searching females. We found that the change in the mating mode affected the level of assortative mating; males mating underground were bigger than those mating on the surface, suggesting active female choice. Given that fiddler crabs experience multiple reproductive cycles, they are prone to showing behavioral plasticity in their mating strategy whenever the payoffs of using different mating modes differ between reproductive events. Our results suggest that the incorporation of different levels of environmental variability may be important in theoretical models aimed at improving our understanding of the evolution of alternative mating tactics and strategies.     

A remarkable case of fiddler crab, Uca spp., alpha diversity in Wallacea

A preliminary attempt was made to quantify the alpha diversity of fiddler crabs (Uca spp.) along a short transect across the interface between an intertidal mudflat and a largely Avicennia mangrove at Ambeua on the Indonesian island of Kaledupa in Sulawesi Tenggara, by means of visual counts within 2 m² quadrats. An astounding diversity of up to six seemingly coexisting species per quadrat—and a total of seven such species within an area of 4 m²—was revealed. Four species of the ecologically equivalent sentinel crabs (Macrophthalmus) were also present in the quadrats. Seven fiddler crab species equates to more than half those known from Wallacea, more than one-third of all those known from Indonesia, and almost one-fifth of the entire Uca fauna of the Indo-West-Pacific.     

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.     

Burrow structure and use in the sand fiddler crab, Uca pugilator (Bosc)

Uca pugilator, the sand fiddler crab, constructs two kinds of burrows in protected, sandy upper-intertidal and supratidal substrates on the west coast of Florida. Temporary burrows are built and used as a refuge by non-breeding crabs during high tide periods and at night when crabs cease feeding in the intertidal zone. Breeding burrows are constructed and defended by courting males and are the site of mating, oviposition and the incubation of eggs by females. Up to three ovigerous females may be accommodated in a single breeding burrow, each female sequestered in a separate terminal chamber. The construction and defence of burrows specialized for breeding may be an adaptive response by males to the preferences females exhibit when selecting a breeding site.