John H. Christy

ECOLOGY AND EVOLUTION OF MATING SYSTEMS OF FIDDLER CRABS (GENUS UCA)

1. General accounts of the natural history and behaviour of fiddler crabs suggest there exist two broad mating patterns in the genus. Most western and Indo‐Pacific species mate on the surface of intertidal substrates near burrows females defend. The sexes associate only briefly during courtship and mating. In contrast, males of many American species court from and defend burrows to which females come for mating. Copulation occurs underground in burrows plugged at the surface; the sexes usually remain together for at least several hours.

Mimicry, Mate Choice, and the Sensory Trap Hypothesis

Sensory traps affect mate choice when male courtship signals mimic stimuli to which females respond in other contexts and elicit female behavior that increases male fertilization rates. Because of the supernormal stimulus effect, mimetic signals may become quantitatively exaggerated relative to model stimuli. Viability selection or a decrease in responsiveness to signals that are exaggerated beyond their peak supernormal effect may limit signal elaboration. Females always benefit by responding to models and they may often benefit by responding to mimetic courtship signals. If the response as a preference is costly, it may be maintained by frequent and strong selection for the response to the model. I review five examples of courtship that illustrate the kinds of studies that can provide evidence of sensory traps. The strategic designs of mimetic courtship signals arise not from selection of responses to them but from selection for responses to models. This results from deceit by mimicry and the evolution of sensory trap responses before the signals that elicit them as preferences.

ADAPTIVE SIGNIFICANCE OF THE TIMING OF LARVAL RELEASE BY CRABS

The adaptive significance of synchronous larval release by marine animals has been elusive. The hatching times of 10 species of intertidal crabs were determined and compared to those expected if crabs release larvae when predation on females, embryos, and newly hatched larvae is least. The safest time to release larvae occurs during the largest-amplitude nocturnal high tides of the lunar month. Crabs throughout the intertidal zone can release larvae near their refuges, and larvae will be transported rapidly at night from shorelines where diurnal planktivores abound. High and middle intertidal species released larvae at this time, which suggests that predation on all three life stages ultimately may synchronize reproduction. Unlike these species, low intertidal crabs are inundated every day, and therefore females could release larvae near refuges daily. Although one low intertidal species did release larvae every day and often during the daytime, two other species released larvae during the safe period. The timing of larval release by low intertidal crabs varies with the vulnerability of their larvae to planktivorous fishes. The hatching times of 46 species worldwide support our contention that predation, primarily on newly hatched larvae, and not other sources of mortality, selects for synchronous hatching by crabs.

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.

Synchronized courtship in fiddler crabs

The apparent paradox posed by the synchronization of mating displays by males competing to attract females has provoked considerable interest among evolutionary biologists,. Such synchronized sexual signalling has only been documented for communicationusing light flashes (bioluminescence) or sound. It has been suggested that the “fundamental reasons that might favour precise adjustments in signal timing relative to that of a particular neighbour could only be compelling for signallers using these two channels”. Here we provide the first quantitative evidence for synchronous production of a conventional visual courtship signal, the movement of a body part.

PLASTICITY, CONSTRAINT, AND OPTIMALITY IN REPRODUCTIVE TIMING'

Synchronous release of gametes or larvae by marine animals may be con- trolled by as many as four environmental cycles thereby enabling an array of reproductive timing patterns. Cohesive scenarios that account for the diversity of reproductive patterns are rare and tests of their adaptive significance have been even rarer. By exploiting plasticity in the timing of larval release, we isolated proximate factors regulating reproductive syn- chrony and provided evidence that predation ultimately may best explain the diversity of hatching patterns by brachyuran crabs. Tides entrain reproductive rhythms by many crabs, and therefore spatial and temporal variation in tides produces intraspecific variation in reproductive patterns. This was demonstrated by determining the timing of larval release of the same or sibling species of intertidal crabs in Pacific semidiurnal and Caribbean mixed semidiurnal tidal regimes on the two coasts of the Republic of Panama. The time of larval release varied during the year in the Caribbean, where entraining physical cycles exhibited complicated changes in phase, but not along the Pacific coast, where the phase relationships among physical cycles varied little year-round. Crabs timed larval release relative to the light-dark, tidal phase, and tidal amplitude cycles, but not the lunar cycle, suggesting that three rhythms determined when larvae were released. For each species we ranked these rhythms by the degree to which larval release kept phase with their entraining physical cycles. The species-specific hierarchies of rhythms we observed match those expected if the time of larval release minimizes predation on females, embryos, and newly hatched larvae. Such hierarchies enable crabs to track phase shifts of cycles in variable tidal en- vironments and may enhance reproductive success across tidal regimes. However, larval release may be timed better in some tidal regimes than others due to differences in the phasing of environmental cycles. In some tidal regimes, larval release cannot be synchro- nized with all three physical cycles during the year, and hierarchies of rhythms may de- termine the timing and duration of breeding.

Attractiveness of sand hoods built by courting male fiddler crabs, Uca musica: test of a sensory trap hypothesis

Courting male fiddler crabs, Uca musica, sometimes build sand hoods at the entrances of their burrows to which they attract females for mating. On average, females visit 17 males in as many minutes before they choose a mate, and they preferentially visit males with hoods. When moving between burrows, fiddler crabs of both sexes sometimes approach and temporarily hide against objects on the surface. Hence, mate-searching females may approach hoods because they resemble (mimic) other objects that crabs approach to reduce their predation risk. We conducted two experiments to test this sensory trap hypothesis. First, we determined whether sexually receptive and nonreceptive female U. musica and nonreceptive female U. stenodactylus, a species that does not build structures, spontaneously approach hoods (replicas), stones, pieces of wood and shells. As predicted by the sensory trap hypothesis, both species, irrespective of sexual receptivity, approached these objects and neither preferred hoods. Second, to determine whether female U. musica show a preference for hoods when they search for a mate, we recorded the frequency with which females approached males with natural hoods, hood replicas, wood, stones and shells. Again as expected, females approached males with these different structures at the same rates. We conclude that hoods are effective mimics of objects that females approach for safety whether they are searching for a mate or not. Males benefit by using this sensory trap because hoods make them more attractive, and receptive females may benefit when they approach hoods because they reduce their mate-search risk.  2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.

Pillar building in the fiddler crab Uca beebei: evidence for a condition-dependent ornament

In the fiddler crab (Uca beebei) males build a small mud pillar next to their burrow which increases their attractiveness to females. Three hypotheses were tested to explain inter-male variation in pillar-building. (1) The benefits of pillar-building are density dependent. The experimental addition of vertical structures did not support this hypothesis as there was no change in the level of pillar-building. (2) There are two classes of males (pillar-builders and non-pillar-builders). This could either be due to an alternative mating strategy, or because pillar building is age or size-dependent. There was also no support for this hypothesis. (3) Pillar-building is an honest signal of male quality dependent on body condition. A food supplementation experiment was performed. Addition of food affected several aspects of male behaviour and resulted in a two fold increase in the number of pillars built between control and food treatments (P < 0.001). However, the percentage of males building pillars did not increase significantly. Pillar building in this species has been attributed to sensory exploitation. Our results indicate that a trait which may well have evolved through sensory exploitation also appears to be condition-dependent. We emphasise that showing that an ornament or behaviour is condition-dependent does not necessarily mean that it evolved through “good gene” processes. However, in terms of its current selective value, pillar building may be maintained through female choice because it acts as a signal of male condition.

Interspecific attractiveness of structures built by courting male fiddler crabs: experimental evidence of a sensory trap

Abstract. Male fiddler crabs Uca musica sometimes build sand hoods and male Uca beebei sometimes build mud pillars next to their burrows to which they attract females for mating. Mate-searching females preferentially approach these structures and subsequently mate with structure builders. Here we show that the preference for structures is not species-specific and argue that it may not have evolved for mate choice. When not near burrows, many species of fiddler crabs approach and temporarily hide near objects, suggesting that hoods and pillars may attract females because they elicit this general predator-avoidance behavior. To test this sensory trap hypothesis we individually released female U. musica, U. beebei and Uca stenodactylus, a non-builder, in the center of a circular array of empty burrows to which we added hoods and pillars and then moved a model predator toward the females. All species ran to structures to escape the predator and the two builders preferred hoods. Next, we put hood replicas on male U. beebei burrows and pillar replicas on male U. musica burrows. When courted, females of both species preferentially approached hoods as they did when chased with a predator. However, males of both species with hoods did not have higher mating rates than males with pillars perhaps because hoods block more of a males visual field so he sees and courts fewer females. Sexual selection may often favor male signals that attract females because they facilitate general orientation or navigation mechanisms that reduce predation risk in many contexts, including during mate search.

Timing of Hatching and Release of Larvae by Brachyuran Crabs: Patterns, Adaptive Significance and Control

Most semiterrestrial, intertidal and shallow subtidal brachyuran crabs that live in tropical and warm temperate estuaries, bays and protected coasts world-wide release their planktonic larvae near the times of nocturnal high tides on the larger amplitude tides in the biweekly or monthly cycles of tidal amplitude. Crab larvae usually emigrate quickly to the sea where they develop to return as postlarvae to settle in habitats suitable for their survival. Predators of larvae are more abundant where larvae are released than where they develop, suggesting that this migration from estuaries to the sea reduces predation on larvae. Crabs with larvae that are relatively well-protected by spines and cryptic colors do not emigrate and often lack strong reproductive cycles, lending support to this explanation. Adults control the timing of the release of larvae with respect to the biweekly and monthly cycles of tidal amplitude by controlling when they court and mate and females control when development begins by controlling when they ovulate and allow their eggs to be fertilized by stored sperm. By changing the time they breed, fiddler crabs (Uca terpsichores) compensate for the effects of spatial and temporal variation in incubation temperature on development rates so that embryos are ready to hatch at the appropriate time. Control of the diel and tidal timing of hatching and of release of larvae varies with where adults live. Females of the more terrestrial species often move from protected incubation sites, sometimes far from water, and they largely control the precise time, both, of hatching and of release of larvae. Females of intertidal species also may influence when embryos begin to hatch. Upon hatching, a chemical cue is released that stimulates the female to pump her abdomen, causing rapid hatching and release of all larvae in her clutch. Embryos, rather than females, largely control hatching in subtidal species, perhaps because females incubate their eggs where they release their larvae. Topics for further study include the mechanism whereby adults regulate the timing of breeding, the mechanisms by which females control development rates of embryos, the nature of communication between females and embryos that leads to precise and synchronous hatching by the number (often thousands) of embryos in a clutch, and the causes of selection for such precision. The timing of hatching and of release of larvae by cold-temperate, Arctic, and Antarctic species and by fully terrestrial and freshwater tropical species has received little attention.