Digest: Ecology and signal structure drive the evolution of synchronous displays in fiddler crabs*

Behaviors are often influenced by both ecology and genetics. Perez et al. tested whether display patterns and the ecology of different species of fiddler crabs influence synchronous waving and whether this a phylogenetic phenomenon. They found that there was no phylogenetic signal in wave display synchronicity, and suggested that signal structure, microhabitat complexity, and different mating systems might instead be the cause. These results support the non-phylogenetic nature of synchronicity that can be observed across animal taxa.     

The evolution of waving displays in fiddler crabs (Uca spp., Crustacea: Ocypodidae)

Male fiddler crabs are commonly recognized by the presence of a single massive claw used in a variety of contexts, including territorial defence, agonistic interactions, and courtship behaviour. The most common behavioural context involving these enlarged chelipeds is their use in waving displays, which are remarkably diverse among species. Although the waving display is one of the most obvious behavioural features of male fiddler crabs, little is known about their main evolutionary trends during the diversification of the genus. The present study employed phylogenetic comparative methods to investigate the evolution of waving behaviour in a sample of 19 species of Uca from Central and North America. Digital recordings were used to quantify the temporal dynamics of waving behaviour in each species. Multivariate ordination methods were used to assess whether different elements of the display showed distinct evolutionary dynamics, particularly with respect to body size and the environment where species are most commonly found. Most of the interspecific variation in displays involves differences in the overall waving velocity, with no correspondence to their local environments, nor their body size. Interestingly, despite the strong concentration of variance in the first two ordination axes, there was no statistically significant evidence for phylogenetic signals in their respective scores. These results suggest that the overall structure of waving displays is evolutionarily labile, at the same time as being concentrated in a few particular axes of variation, possibly indicating evolution along lines of least resistance. The approach employed in the present study highlights the utility of phylogenetic comparative methods for elucidating the evolution of complex behavioural characteristics, such as the waving display in male fiddler crabs. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106 , 307–315.     

The functions of multiple visual signals in a fiddler crab

In many species, it is common for animals to have multiple signals within one channel of communication. Multiple signals may, however, be inefficient if they are redundant in nature. Identifying the functional significance of these multiple signals is therefore important if we are to understand the evolution of such elaborated behaviours. We proposed to identify the roles of movement-based multiple signals in a model animal system. Male fiddler crabs wave their sexually dimorphic enlarged claw during social interactions. Some species present multiple signals, where the level of complexity of the movement changes. Males of Austruca mjoebergi can perform a double wave consisting of a high- followed by a low-elevation lifting of the claw, or a single wave consisting of the high-elevation movement alone. We first investigated structural differences between the double and single wave types, and found that single waves were lower in elevation than double waves. We then explored the adaptive meaning of the wave types by manipulating the social context in which males wave. We found that double waves were given in all contexts and in higher proportions at long distances, suggesting a function of broadcasting male location. Single waves, on the other hand, were mainly given at close range and in the presence of conspecifics, suggesting intraspecific communication. Female presence elicited the highest number and proportion of single waves, a likely result of a female preference for higher wave rates. Finally, we point out that there is an element of interaction between wave types that deserves future attention. This paper is an important contribution to expand our understanding of the adaptive meaning of multiple visual signals and help reach a unified theory of their evolution.     

Phylogenetic autocorrelation and heritability of geographic range size,shape and position of fiddler crabs,genus Uca (Crustacea,Decapoda)

The aim of this study was to evaluate the levels of phylogenetic heritability of the geographical range size, shape and position for 88 species of fiddler crabs of the world, using phylogenetic comparative methods and simulation procedures to evaluate their fit to the neutral model of Brownian motion. The geographical range maps were compiled from literature, and range size was based on the entire length of coastline occupied by each species, and the position of each range was calculated as its latitudinal and longitudinal midpoint. The range shape of each species was based in fractal dimension (box‐counting technique). The evolutionary patterns in the geographical range metrics were explored by phylogenetic correlograms using Moran’s I autocorrelation coefficients, autoregressive method (ARM) and phylogenetic eigenvector regression (PVR). The correlograms were compared with those obtained by simulations of Brownian motion processes across phylogenies. The distribution of geographical range size of fiddler crabs is right‐skewed and weak phylogenetic autocorrelation was observed. On the other hand, there was a strong phylogenetic pattern in the position of the range (mainly along longitudinal axis). Indeed, the ARM and PVR evidenced, respectively, that ca. 86% and 91% of the longitudinal midpoint could be explained by phylogenetic relationships among the species. The strong longitudinal phylogenetic pattern may be due to vicariant allopatric speciation and geographically structured cladogenesis in the group. The traits analysed (geographical range size and position) did not follow a Brownian motion process, thus suggesting that both adaptive ecological and evolutionary processes must be invoked to explain their dynamics, not following a simple neutral inheritance in the fiddler‐crab evolution.     

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.     

Keeping up appearances: male fiddler crabs wave faster in a crowd

Courtship displays are often energetically and temporally costly as well as highly conspicuous to predators. Selection should therefore favour signalling tactics that minimize courtship costs while maintaining or increasing signal attractiveness. In fiddler crabs, males court females by waving their one greatly enlarged claw in a highly conspicuous and costly display. Here, we investigate whether courting males adjust their wave rate, and therefore the cost of courtship, to the current level of competition. We show that display rate increases as competition increases and that when competition is removed, males reduce their display rate by 30 per cent. These results suggest that male fiddler crabs actively reduce the cost of courtship by adjusting their wave rate in response to the immediate level of competition.     

Variability of a dynamic visual signal: the fiddler crab claw-waving display

Fiddler crabs use elaborate, species-specific claw-waving displays to communicate with rivals and mates. However, detailed comparative studies of fiddler crab signal structure and structural variations are lacking. This paper provides an analysis of the claw-waving displays of seven Australian species of fiddler crab, Uca mjoebergi, U. perplexa, U. polita, U. seismella, U. signata, U. elegans and U. vomeris. We used digital video to record and analyse the fine-scale spatiotemporal properties of these movement-based visual signals. We found that the structure and timing of the displays is species-specific, exhibiting inter-specific differences that follow phylogenetic relationships. The displays showed intra-specific variation according to individual identity, geographic location and fine-scale behavioural context. The observed differences and variations are discussed in the light of the evolutionary forces that may shape their design.     

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.     

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.     

Behavioral patterns of two fiddler crab species Uca rapax and Uca tangeri in a seminatural mangrove system

Zoos increasingly transform their exhibitions from traditional one‐species enclosures to more natural exhibits, that is, environments that capture part of an ecosystem including a selection of animals and plants that occur there. Thus, enhancing the experience of its human visitors while also allowing its residents to possibly show more natural behavior. In 2017 Royal Burger's Zoo (Arnhem, The Netherlands) created and opened a mangrove‐like environment containing fiddler crabs. Fiddler crabs display a broad range of behaviors, and this research examines which wild‐type behavior and behavioral patterns can be observed on a seminatural mudflat. The behavior shown by Uca rapax and Uca tangeri on the mudflat was counted each hour between 07:00 and 17:00. An asymmetric tidal regime was present in the enclosure including two high water periods. Various known fiddler crab behaviors, including waving and combat, were observed but no copulation. A clear pattern in exposed crabs on the mudflat was found, with low numbers visible in the early morning and the highest numbers present in the early afternoon, while number of visitors did not have a significant effect on this pattern. Interestingly, the highest abundances were not observed around the ebbing tide (07:00–09:00), as observed in the wild, but somewhat later, possibly due to the asymmetric tidal scheme or the interaction of tidal and daily rhythms. This study shows that in captivity, fiddler crabs indeed show a range of natural behaviors which is linked to the tidal and possibly daily rhythm as well.     

Female Choice in the Synchronously Waving Fiddler Crab Uca annulipes

In the fiddler crab, Uca annulipes, males attract receptive females into their burrows by waving their greatly enlarged major claw. We have previously shown that males clustered around a female wave in close synchrony. Females may have a preference for leading signals and synchronised waving may arise as an epiphenomenon of competition between males to signal first. Indeed, the males in clusters that females approach and visit in their burrows are more likely to produce leading waves than are their neighbours. Here we document two other differences in the waving behaviour of visited males and their neighbours. First, visited males complete the downward component of the wave more rapidly than their neighbours. Second, the interval between the end of one wave and the start of the next is shorter for visited males. How can waving be synchronous if visited males wave faster than their neighbours? While only 9% (40/431) of waves by neighbours did not overlap those of the visited male, 22% (110/501) of visited male waves did not overlap the wave of a focal neighbour (111 visited male-neighbour dyads). Hence, while overlapping waves are nearly synchronous, visited males produce additional, ‘nonoverlapping’ waves that result in a higher wave rate than that of their neighbours.     

The latitudinal,but not the longitudinal,geographic range positions of haematophagous ectoparasites demonstrate historical signatures

We tested whether geographic range position of fleas parasitic on small mammals in the Palearctic is affected by environmental niche conservatism or geographic range conservatism by measuring phylogenetic signal in range centroids and boundaries. We predicted that stronger phylogenetic signal in latitudinal than longitudinal range positions would indicate the important role of niche conservatism as a driver of the evolution of fleas’ geographic ranges. Phylogenetic signals in geographic range positions were measured across 120 species, as well as within five flea lineages (subfamily/family rank) of different evolutionary ages. To investigate the temporal pattern of the geographic range position’s evolution, we fitted the phylogenetic patterns in the geographic coordinates of range centroids and border extremes to four models of trait evolution. We consistently detected significant phylogenetic signals in the latitudes of the range centroids and the northern range borders. The latitudes of the southern range borders and the longitudes of the eastern/western borders demonstrated phylogenetic signals less often, whereas no signal was found for the longitudes of the range centroids. The phylogenetic signal in range position was more pronounced in younger lineages. The phylogenetic signal indices mainly suggested the evolution of range positions according to the Brownian motion model, whereas the best fit was often provided by the Orstein-Uhlenbeck model. This contradiction forced us to invoke a parsimonious explanation that the phylogenetic signal in range positions results from the interplay between the footprint of the speciation pattern and limited dispersal from the ancestral ranges.     

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.     

Habitat partitioning between prey soldier crab Mictyris brevidactylus and predator fiddler crab Uca perplexa

Interaction and habitat partition between the soldier crab Mictyris brevidactylus (prey) and the fiddler crab Uca perplexa (predator) were examined at a sandy tidal flat on Okinawa Island, Japan, where they co-occur. Both live in dense colonies. When the soldier crabs were released in the densely populated habitat of the fiddler crab, male fiddler crabs, which maintain permanent burrows in hard sediment, preyed on small soldier crabs and repelled large ones. Thus, the fiddler crabs prevented the soldier crabs from trespassing. It was also observed whether soldier crabs burrowed successfully when they were released 1) where soldier crab burrows just under the sand were abundant, 2) in a transition area between the two species, 3) an area without either species, and 4) where artificial tunnels simulated soldier crabs' feeding tunnels were made by piling up sand in the area lacking either species. In contrast to the non-habitat area, many soldier crabs burrowed in the sediment near the release point in the tunnel, transition and artificial tunnel areas. This indicates that the feeding tunnels on the surface attracted other crabs after emergence. When the large male fiddler crabs were transplanted into the artificial burrows made in soft sediment of the soldier crab habitat, all left their artificial burrows by 2 days. In the fiddler crab habitat, however, about one-third of the transplanted male fiddler crabs remained in the artificial burrows after 3 days. The soldier crabs regularly disturb the sediment by the up and down movement of their burrow (small air chamber) between tides. This disturbance probably prevents the fiddler crab from making and occupying permanent burrows. Thus, it appears that these crabs divide the sandy intertidal zone by sediment hardness and exclude each other by different means.     

Choosing a mate in a high predation environment: Female preference in the fiddler crab Uca terpsichores

The interplay between a receiver's sensory system and a sender's courtship signals is fundamental to the operation of sexual selection. Male courtship signals that match a female receiver's preexisting perceptual biases can be favored yet the message they communicate is not always clear. Do they simply beacon the male's location or also indicate his quality? We explored this question in a species of fiddler crab Uca terpsichores that courts under elevated predation risk and that mates and breeds underground in the safety of males' burrows. Sexually receptive females leave their own burrows and are thereby exposed to avian predators as they sequentially approach several courting males before they choose one. Males court by waving their single greatly enlarge claw and sometimes by building a sand hood next to their burrow entrance. Hoods are attractive because they elicit a risk‐reducing orientation behavior in females, and it has been suggested that claw waving may also serve primarily to orient the female to the male. If the wave communicates male quality, then females should discriminate mates on the basis of variation in elements of the wave, as has been shown for other fiddler crabs. Alternatively, variation in elements of the claw waving display may have little effect on the display's utility as a beacon of the location of the male and his burrow. We filmed courting males and females under natural conditions as females responded to claw waving and chose mates. Analysis of the fine‐scale courtship elements between the males that females rejected and those they chose revealed no differences. When predation risk during courtship is high, males' courtship displays may serve primarily to guide females to safe mating and breeding sites and not as indicators of male quality apart from their roles as beacons.     

The effect of audience on intrasexual interaction in the male fiddler crab, <Emphasis Type="Italic">Uca maracoani</Emphasis> (Latreille 1802–1803, Decapoda,Ocypodidae)

Animal communication occurring in wide networks can involve signals sent to several receivers. The animals composing the audience may affect how individuals display during an interaction and may change the message that is sent. In this study, we investigated whether the presence of a conspecific affected the intensity of agonistic interaction between male fiddler crabs, Uca maracoani. Pairs of males of the same size were observed when in the presence of a male, a female or no crab as audience. We found that if there is a female audience, males became more aggressive and interacted the most. Also, the female audience leads to an increase in incidence of male foaming, possibly indicating predisposition for mating. If the audience was a male or if there was no audience, there was no significant difference in interaction. These results indicate that the presence of an audience affects the way male fiddler crabs interact and the type of displays they show. Therefore, the context seems to guide the fiddler crab behavior in terms of how they perform in order to send information about themselves to conspecifics.     

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.     

Independent and interactive effects of two facilitators on their habitat‐providing host plant,Spartina alterniflora

The role of habitat‐providing species in facilitating associated species abundance and diversity is recognized as a key structuring force in many ecosystems. Reciprocal facilitation by associates, often involving multiple species, can be important for the maintenance of the host species. As with other multi‐species interactions (e.g. multiple predator effects), non‐additive relationships may be common among these associates, yet relatively few studies have examined potential interactions among multiple facilitator species. We combined field surveys and a mesocosm experiment to examine the independent and interactive effects of two co‐occurring facilitator species, ribbed mussels Geukensia demissa and fiddler crabs Uca pugilator, on their host salt marsh plant species, cordgrass Spartina alterniflora. We also experimentally examined how these relationships varied across different host plant genotypes. Overall, facilitator effects increased with increasing facilitator density. There was a significant interaction between mussel and fiddler crab presence, indicating that the effects of each species on cordgrass were dependent on the presence of the other facilitator species. In addition, there were strong interactions among mussels, fiddler crabs, and plant genotype, with greater variation in the performance of individual genotypes when fiddler crabs were absent. Our work reinforces the importance of considering multiple responses when assessing the functional redundancy of co‐occurring facilitators, as species are seldom completely redundant across the range of services they provide. It also highlights that the strength and direction of species interactions can vary due to genetic variation within the interacting species.     

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.     

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.