Tuning breadth and sex-specific sensitivity in chemosensory neurons of male and female Uca pugnax

Chemosensory neurons of female fiddler crabs (genus Uca) display greater sensitivity to mixtures of food-related stimuli than do neurons in males. This phenomenon represents an interesting contrast to other sex-specific systems, which tend to be in response to cues associated with mating and parental care. This study examined the responses of chemosensory neurons in males and females to ten individual stimuli to determine if sex-specific responses were restricted to a few key compounds, or if the heightened sensitivity of females was broadly distributed. Neurons in males and females responded well to all stimuli, and although fiddler crabs are primarily herbivorous, highly efficacious physiological stimulants included amino acids and amines as well as carbohydrates most closely associated with plant material. The chemosensory neurons are characterized by broad tuning and relatively high response thresholds, when compared to other crustaceans. Most importantly, the investigations revealed a robust pattern in which female neurons displayed elevated responses to all stimuli. Tuning breadth was not shown to be sex-specific, nor were there detectable differences in over-all response profiles. The most likely explanation for these patterns is that the broad sex-specificity in Uca is produced via fundamental alterations in cellular properties associated with chemosensory transduction. Accepted: 29 June 1999     

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.     

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.     

Even Weak Males Help Their Neighbours: Defence Coalitions in a Fiddler Crab

Large male fiddler crabs sometimes help smaller neighbours to defend their territories against intruders. These coalitions occur when the helper is likely to defeat the intruder (helper larger than intruder) and the neighbour is likely to lose his territory without help (intruder larger than neighbour). Previous studies of coalitions have excluded males with regenerated claws. Such claws are weaker weapons that make the bearer competitively inferior. Here, we show that male Uca annulipes with regenerated claws are as likely as males with original claws to help their neighbours in territory defence, even though, as weaker males they potentially pay greater costs, being more likely to lose their undefended burrow. We suggest that males with regenerated claws gain greater benefits from retaining a current, small neighbour and that, as in non‐coalition fights, the regenerated claw acts as a visual bluff in the early stages of combat. Furthermore, we show that intruders with regenerated or original claws are equally likely to be attacked by a ‘helping’ neighbour. This bolsters the argument that males cannot visually differentiate between original and regenerated claws.     

Synchronous waving in two species of fiddler crabs

In the fiddler crabs Uca saltitanta and Uca perplexa, males attract mates by waving their enlarged claws. We show that in both species waving is closely synchronised between neighbouring males in clusters, both in the presence of mate-searching females and in their absence. Wandering females visit those males in the cluster that produce more waves at faster wave rates. In U. perplexa, they also selectively visit those males that produce the greatest number of leading waves. Synchronous waving may be the result of a precedence effect causing male competition to produce leading signals.     

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.     

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.     

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.     

Male size and reproductive success in the communal courtship system of the fiddler crab Uca rapax

Reproductive success of male fiddler crabs Uca rapax depends on the numbers of females a male can attract, and the fecundity of these females. The latter correlates directly with fenale size. The size of a female in a mated pair is directly correlated with the size of the male. Therefore, older larger males experience greater reproductive success than smaller younger males. Females appear to be highly selective in mating, while males are not. The question of why females should select a male whose size is correlated with hers cannot be answered from the present study.     

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.     

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.     

The fiddler crab Uca mjoebergi uses colour vision in mate choice

Although the role of colour in mate choice is well known, few tests of colour vision have been based on mating behaviour. Females of the fiddler crab Uca mjoebergi have recently been shown to use claw coloration to recognize conspecific males. In this study I demonstrate that the females use colour vision for this task; preferentially approaching yellow claws over grey claws regardless of their intensity while failing to discriminate between yellow claws differing in intensity. This is one of only a handful of studies confirming the involvement of colour vision in mate choice and the first conclusive evidence in fiddler crabs.     

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 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.     

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.     

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.     

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.     

Predation by red-jointed fiddler crabs on congeners: interaction between body size and positive allometry of the sexually selected claw

The enlarged (major) claw of male fiddler crabs is used in contestsover breeding burrows and is waved to attract females. We recentlydiscovered that males of the red-jointed fiddler crab, Uca minax,also use the claw to kill smaller-sized fiddler crabs, U. pugnaxand U. pugilator, with which they co-occur in Atlantic coastsalt marshes. Large U. minax males use walking legs or the enlargedclaw to capture prey feeding on moist sand flats. On sand flats,small U. minax males and females are much less common than largemales, suggesting that large males move onto sand flats to seekprey. Males of prey species use the major claw against attackingpredators and, consequently, are more likely than females toescape. In laboratory experiments, large U. minax males weremore likely to attack and kill small-clawed males and femalesthan large-clawed males, consistent with a preference for morevulnerable, less threatening prey. The size of the major clawis a positive allometric function of body size. The allometricfunction varies little among species. Also, the mechanical advantageand indices of closing speed and closing force of the majorclaw, when corrected for body size, are not consistently greaterin U. minax relative to prey species. Thus, predation by U.minax males may reflect the opportunity afforded by larger bodysize and positive allometric growth, which result in a majorclaw that is more massive than the prey it is directed against.     

Shell use by juvenile fiddler crabs Uca pugnax and U. pugilator

The present study documents for the first time shell use by juvenile fiddler crabs in the salt marsh. Twenty visits were made to six salt marsh sites at Tybee Island, Georgia between 2007 and 2009. One hundred empty Littorina irrorata shells were collected at each site on each field trip. Juvenile carapace width was measured, crabs sexed, and species identification completed using RFLP analysis. Shell use of up to 79% was observed. Two species of fiddler crabs were found in empty shells, Uca pugnax and U. pugilator. U. pugnax was the dominant species at all sites representing 62-84% of the juvenile fiddler crab population. Juvenile sex ratios were female-biased (1.7:1) at all six sites. Juvenile size did not vary significantly between species but males of both species were significantly larger than females. Size frequency distribution of carapace width revealed that shell use varied with size and sex. In the 3 to 4 mm size class, juvenile females outnumbered juvenile males in empty L. irrorata shells while in the 5 to 6 mm size class and greater, juvenile males outnumbered juvenile females in shells. Significantly more juvenile fiddler crabs were found in empty shells during flood than ebb tide at 3 of the sites. This discovery illuminates the resourcefulness of juvenile fiddler crabs and provides another mechanism that might enhance survival.     

Burrow ornamentation in the fiddler crab (Uca leptodactyla): female mate choice and male–male competition

Non-biological ornamentation is found in the nests and burrows of different kinds of animals. We evaluated here whether sand hoods constructed by male fiddler crabs (Uca leptodactyla) are one of the signals used by males to attract females during courtship. We observed females when they were walking among the males, and we quantified the proportion of females that visited male burrows with and without ornamentation and the choice to stay in a male’s burrow. Females visited more burrows with hoods than burrows without hoods, and they chose significantly more builder males. Male investment in ornamentation nevertheless decreased when the proportion of females increased in the area. Male investment was not correlated with the proportion of non-builder males nearby, but was positively correlated with overall density. The density sex ratio, however, was more male-biased in high-density than in low-density areas suggesting that even if building attracts females, the function could be related to male competition for mates.