Costs and compensation in zooplankton pigmentation under countervailing threats of ultraviolet radiation and predation.

Evolutionary responses to opposing directions of natural selection include trade-offs, where the phenotype balances selective forces, and compensation, where other traits reduce the impact of one selective force. Zooplankton pigmentation protects from ultraviolet radiation (UVR) but attracts visual predators. This trade-off is understudied in the ocean where planktonic larvae in surface waters face ubiquitous UVR and visual predation threats. We tested whether crab larvae can behaviorally reduce UVR risk through downward swimming or expansion of photoprotective chromatophores. Then we examined whether more pigmented larvae are more heavily predated by silverside fish under natural sunlight in the tropics in three UVR treatments (visible light, visible + UVA, visible + UVA + UVB). Lastly, we tested the behavioral chromatophore response of larvae to predation threats in two light treatments. Armases ricordi avoided surface waters after exposure to sunlight with UVR. Armases ricordi, Armases americanum, and Eurypanopeus sp. consistently expanded chromatophores in UVR or visible light, while Mithraculus sculptus and Mithraculus coryphe showed no response. Fish preferred pigmented larvae on sunnier days in visible light lacking UVR. Lastly, both M. coryphe and M. sculptus unexpectedly expanded chromatophores in fish cues, but responses were inconsistent over trials and across light treatments. The more consistent larval responses to UVR than to predator cues and the lack of predator preferences in natural light conditions suggest that UVR may have a stronger influence on pigmentation than predation. This study improves our understanding of planktonic adaptation to countervailing selection caused by visual predation and exposure to UVR.

Multiple and Extra-Pair Mating in a Pair-Living Hermaphrodite, the Intertidal Limpet Siphonaria gigas.

Pair-living is a common social system found across animal taxa, and the relationship between pair-living and reproduction varies greatly among species. Siphonaria gigas, hermaphroditic pulmonate gastropods, often live in pairs in the rocky intertidal zone of the tropical Eastern Pacific. Combining genetic parentage analysis using four polymorphic microsatellite loci with behavioral observations from a 10-week field study, we provide the first description of the mating system of a Siphonaria species incorporating genetic data. S. gigas mated both within-pair and extra-pair and three out of four paired S. gigas individuals produced egg masses with extra-pair paternity. Multiple paternity was detected, but at a relatively low frequency (19% of egg masses) compared to other marine gastropods. Behavioral data indicate one potential advantage of pair-living: paired S. gigas produced almost twice as many egg masses as their solitary counterparts over four reproductive cycles. These observations, together with constraints on the movement of S. gigas, suggest that pairing may ensure mate access and increase reproductive success.

Apareamiento múltiple y extrapareja en un hermafrodita que vive en pareja, la lapa intermareal Siphonaria gigas (Multiple and extra-pair mating in a pair-living hermaphrodite, the intertidal limpet Siphonaria gigas). Vivir en pareja es un sistema social común que se encuentra en los taxones de animales, y la relación entre la vida en pareja y la reproducción varía mucho entre las especies. Siphonaria gigas, gasterópodos pulmonados y hermafroditas, a menudo viven en parejas en la zona rocosa intermareal del Pacífico oriental tropical. Combinando el análisis de parentesco genético utilizando cuatro loci de microsatélites polimórficos con observaciones de comportamiento de un estudio de campo de 10 semanas, proporcionamos la primera descripción del sistema de apareamiento de una especie Siphonaria que incorpora datos genéticos. S. gigas se apareó tanto dentro como fuera de la pareja, y tres de cada cuatro individuos de S. gigas emparejados produjeron masas de huevo con paternidad extrapareja. Se detectó paternidad múltiple, pero a una frecuencia relativamente baja (19% de las masas de huevo) en comparación con otros gasterópodos marinos. Los datos de comportamiento indican una ventaja potencial de la vida en pareja: S. gigas emparejado produjo casi el doble de masas de huevo que sus contrapartes solitarias durante cuatro ciclos reproductivos. Estas observaciones, junto con el movimiento restringido de S. gigas, sugieren que el emparejamiento puede garantizar el acceso de pareja y aumentar el éxito reproductivo. Translated to Spanish by YE Jimenez (yordano_jimenez@brown.edu).

Photoprotective benefits of pigmentation in the transparent plankton community: a comparative species experimental test.

Plankton live under the countervailing selective pressures of predation and ultraviolet radiation (UVR). In lakes, zooplankton are transparent reducing visibility to predatory fishes but are pigmented in the absence of fishes, hypothetically reducing UVR damage. In the sea, planktivorous fishes are widespread, so plankton typically are transparent and ascend to productive surface waters at night to forage and descend during the day to reduce visibility to predators. However, larvae of some species face the unique constraint of traveling in surface currents in the daytime during migrations between adult and larval habitats. We would expect these larvae to be transparent since companion studies demonstrated increased predation risk of pigmented larvae under strong sunlight. Paradoxically, larvae range from being darkly to lightly pigmented. We hypothesize that some larvae are more heavily pigmented to reduce UVR damage, while other species travelling in subsurface currents with low UVR might be more transparent. Linking larval morphology to depth-dependent selective pressures would add a key element to help improve predictions of larval vertical distributions, which are important for simulating larval transport trajectories. We quantitatively tested the hypothesis that selection may have favored photoprotective pigmentation for larvae in the predominantly transparent plankton community while testing the differential effects of UVA and UVB radiation. We measured larval pigmentation of 12 species of crabs and exposed them to visible light only, visible + UVA, or visible + UVA + UVB in the tropics. Controlling for phylogeny, more pigmented species survived UVR better than less pigmented species, especially on sunnier days, though intraspecific comparisons for four species were equivocal. Most species died even from UVA exposure, which has long been regarded as relatively harmless despite penetrating deeper underwater than UVB. Thus, we demonstrate with a phylogenetically controlled analysis that crab larvae are pigmented in the predominantly transparent planktonic community to protect from UVR, improving our understanding of the selective forces acting on animal coloration and the factors determining planktonic distributions, survival, and dispersal. This linkage of morphology with susceptibility will be important for developing mechanistic models of environmental stress responses to better predict larval dispersal in current and future climates.

Specialized morphology corresponds to a generalist diet: linking form and function in smashing mantis shrimp crustaceans.

Many animals are considered to be specialists because they have feeding structures that are fine-tuned for consuming specific prey. For example, "smasher" mantis shrimp have highly specialized predatory appendages that generate forceful strikes to break apart hard-shelled prey. Anecdotal observations suggest, however, that the diet of smashers may include soft-bodied prey as well. Our goal was to examine the diet breadth of the smasher mantis shrimp, Neogonodactylus bredini, to determine whether it has a narrow diet of hard-shelled prey. We combined studies of prey abundance, feeding behavior, and stable isotope analyses of diet in both seagrass and coral rubble to determine if N. bredini's diet was consistent across different habitat types. The abundances of hard-shelled and soft-bodied prey varied between habitats. In feeding experiments, N. bredini consumed both prey types. N. bredini consumed a range of different prey in the field as well and, unexpectedly, the stable isotope analysis demonstrated that soft-bodied prey comprised a large proportion (29-53 %) of the diet in both habitats. Using a Bayesian mixing model framework (MixSIAR), we found that this result held even when we used uninformative, or generalist, priors and informative priors reflecting a specialist diet on hard-shelled prey and prey abundances in the field. Thus, contrary to expectation, the specialized feeding morphology of N. bredini corresponds to a broad diet of both hard-shelled and soft-bodied prey. Using multiple lines of study to describe the natural diets of other presumed specialists may demonstrate that specialized morphology often broadens rather than narrows diet breadth.

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.

Uca (Petruca), a new subgenus for the rock fiddler crab Uca panamensis (Stimpson, 1859) from Central America, with comments on some species of the American broad-fronted subgenera.

Among the fiddler crabs from the Americas, Uca panamensis (Stimpson, 1859) (Crustacea: Decapoda: Ocypodidae) is unusual in its behavior and ecology, living in stony habitats rather than sandy or muddy substrates. This species also has several unusual morphological characters of the carapace and major and minor chelae, and had been placed in either the subgenera Minuca Bott, 1954, or Leptuca Bott, 1973. The armature at the inner corner of the orbital floor, as well as the morphology of the urocardiac ossicles of the gastric mill of U. panamensis, are, however, plesiomorphic characters, and are closer to the condition in species belonging the subgenera Uca and Afruca. Phylogenetic relationships, based on mitochondrial 16S rDNA and cytochrome oxidase subunit I, and nuclear 28S rDNA, supported by its unusual morphological features indicate that this species belongs to its own subgenus. A new subgenus Uca (Petruca) subgen. nov. is herein established for U. panamensis. In addition, the status of Uca thayeri Rathbun, 1900, U. umbratila Crane, 1941, U. virens Salmon & Atsaides, 1968, and U. longisignalis Salmon & Atsaides, 1968, are revised and discussed based on a reappraisal of their phylogenetic relationships.

Target Detection Is Enhanced by Polarization Vision in a Fiddler Crab.

We are constantly surprised by the ability of relatively simple animals to perform precise visually guided movements within complex visual scenes, often using eyes with limited resolution. Exceptional examples include the capture of airborne prey by dragonflies, the learning flights of bees and wasps, and the tracking of conspecifics by crabs on intertidal mudflats. Most studies have focused on how animals do this using sensitivity to intensity or color. However, it is increasingly evident that a third ability, polarization vision, may contribute to such tasks. In many insects, polarization-sensitive photoreceptors are confined within an area of the eye known as the dorsal rim, which detects the polarized sky pattern specifically for navigation. However, some animals, including fiddler crabs, are sensitive to the polarization of light across the majority of their image-forming eyes, potentially allowing them to use polarization information to increase perceived contrast for general visual tasks. Investigations into the use of polarization image-parsing by animals have largely been confined to laboratory settings under artificial lighting. This approach can occasionally mislead if the lighting conditions are different from natural. This study presents the first behavioral evidence from the natural context for a function of polarization image parsing. Using experimental manipulations in wild populations of the fiddler crab Uca stenodactylus, we provide evidence that these animals use their polarization vision to enhance contrast in their visual environment, thereby increasing their ability to detect and respond to objects on the mudflat surface.

Reproducing on time when temperature varies: shifts in the timing of courtship by fiddler crabs.

Many species reproduce when conditions are most favorable for the survival of young. Numerous intertidal fish and invertebrates release eggs or larvae during semilunar, large amplitude, nocturnal tides when these early life stages are best able to escape predation by fish that feed near the shore during the day. Remarkably, some species, including the fiddler crabs Uca terpsichores and Uca deichmanni, maintain this timing throughout the year as temperature, and thus the rate of embryonic development, vary. The mechanisms that allow such precision in the timing of the production of young are poorly known. A preliminary study suggested that when temperature decreases, U. terpsichores mate earlier in the tidal amplitude cycle such that larvae are released at the appropriate time. We tested this idea by studying the timing of courtship in U. terpsichores and U. deichmanni as temperature varied annually during two years, at 5 locations that differed in the temperature of the sediment where females incubate their eggs. Uca terpsichores courted earlier at locations where sediment temperature declined seasonally but not where sediment temperature remained elevated throughout the year. In contrast, clear shifts in courtship timing were not observed for U. deichmanni despite variation in sediment temperature. We discuss other mechanisms by which this species may maintain reproductive timing. These two species are likely to be affected differently by changes in the frequency and intensity of cold periods that are expected to accompany climate change.

Evolutionary variation in the mechanics of fiddler crab claws.

BACKGROUND: Fiddler crabs, genus Uca, are classic examples of how intense sexual selection can produce exaggerated male traits. Throughout the genus the enlarged "major" cheliped (claw) of the male fiddler crab is used both as a signal for attracting females and as a weapon for combat with other males. However, the morphology of the major claw is highly variable across the approximately 100 species within the genus. Here we address variation, scaling, and correlated evolution in the mechanics of the major claw by analyzing the morphology and mechanical properties of the claws of 21 species of fiddler crabs from the Pacific, Gulf and Atlantic coasts of the Americas. RESULTS: We find that the mechanics that produce claw closing forces, the sizes of claws and the mechanical strength of the cuticle of claws are all highly variable across the genus. Most variables scale isometrically with body size across species but claw force production scales allometrically with body size. Using phylogenetically independent contrasts, we find that the force that a claw can potentially produce is positively correlated with the strength of the cuticle on the claw where forces are delivered in a fight. There is also a negative correlation between the force that a claw can potentially produce and the size of the claw corrected for the mass of the claw. CONCLUSIONS: These relationships suggest that there has been correlated evolution between force production and armoring, and that there is a tradeoff between claw mechanics for signaling and claw mechanics for fighting.

The design of a beautiful weapon: compensation for opposing sexual selection on a trait with two functions.

Male fiddler crabs, genus Uca, have one greatly enlarged claw with which they court females and threaten and fight other males. Longer claws are more effective signals but are thought to be less effective weapons because the relative closing force at the tip of the claw decreases with claw length. We studied claw morphology and fighting in Uca terpsichores and Uca beebei and found a mechanism that may resolve opposing selection for signaling and fighting ability. When males fought they delivered gripping forces not at the tips but at the tubercles on the inner margins of their claws' fingers. As claws grow, these tubercles remain relatively close to the apex of the gape. Consequently, the mechanical advantage that governs the forces that can be delivered at these tubercles decreases only slightly with increasing claw length allowing the claw to be an effective signal and a powerful weapon. Animal weapons are exceptionally diverse in form and detail of armature and the causes of this diversity are poorly understood. We suggest that the designs of weapons may often reflect compensatory patterns of growth and placement of armature that enhances the weapon's overall utility for multiple uses in competition for mates.

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.

The strength of a female mate preference increases with predation risk.

When females search for mates and their perceived risk of predation increases, they less often express preferences for males that use conspicuous courtship signals, relaxing sexual selection on production of these signals. Here, we report an apparent exception to this general pattern. Courting male fiddler crabs Uca beebei sometimes build pillars of mud at the openings to their burrows in which crabs mate. Females visit several males before they choose a mate by staying and breeding in their burrows, and they preferentially visit males with pillars. Previous studies suggested that this preference is based on a visual orientation behaviour that may reduce females' risk of predation while searching for a mate. We tested this idea by determining whether the female preference for males with pillars increases with perceived predation risk. We attracted avian predators to where crabs were courting and measured the rates that sexually receptive females visited courting males with and without mud pillars. Under elevated risk, females continued to search for mates and they showed a stronger relative preference for males with pillars. Thus, when predation risk is high, females may continue to express preferences that are under natural selection because they help females avoid predation, strengthening sexual selection for use of the preferred signal.

A preference for a sexual signal keeps females safe.

Predation is generally thought to constrain sexual selection by female choice and limit the evolution of conspicuous sexual signals. Under high predation risk, females usually become less choosy, because they reduce their exposure to their predators by reducing the extent of their mate searching. However, predation need not weaken sexual selection if, under high predation risk, females exhibit stronger preferences for males that use conspicuous signals that help females avoid their predators. We tested this prediction in the fiddler crab Uca terpsichores by increasing females' perceived predation risk from crab-eating birds and measuring the attractiveness of a courtship signal that females use to find mates. The sexual signal is an arching mound of sand that males build at the openings of their burrows to which they attract females for mating. We found that the greater the risk, the more attractive were males with those structures. The benefits of mate preferences for sexual signals are usually thought to be linked to males' reproductive contributions to females or their young. Our study provides the first evidence that a female preference for a sexual signal can yield direct survival benefits by keeping females safe as they search for mates.