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.     

Molecule capture by olfactory antennules: Mantis shrimp

 A critical step in the process of olfaction is the movement of odorant molecules from the environment to the surface of a chemosensory structure. Many marine crustaceans capture odorant molecules with arrays of chemosensory sensilla (aesthetascs) on antennules that they flick through the water. We developed a model to calculate molecule flux to the surfaces of aesthetascs in order to study how the size, aesthetasc spacing, and flick kinematics of olfactory antennules affect their performance in capturing molecules from the surrounding water. Since the three-dimensional geometry of an aesthetasc-bearing antennule is complex, dynamically-scaled physical models can often provide an efficient method of determining the fluid velocity field through the array. Here we present a method to optimize the incorporation of such measured velocity vector fields into a numerical simulation of the advection and diffusion of odorants to aesthetasc surfaces. Furthermore, unlike earlier models of odorant interception by antennae, our model incorporates odorant concentration distributions that have been measured in turbulent ambient flows. By applying our model to the example of the olfactory antennules of mantis shrimp, we learned that flicking velocity can have profound effects on odorant flux to the aesthetascs if they operate in the speed range in which the leakiness of the gaps between the aesthetascs to fluid movement is sensitive to velocity. This sensitivity creates an asymmetry in molecule fluxes between outstroke and return stroke, which results in an antennule taking discrete samples in space and time, i.e. “sniffing”. As stomatopods grow and their aesthetasc Reynolds number increases, the aesthetasc arrangement on the antennule changes in a way that maintains these asymmetries in leakiness and molecule flux between the outstroke and return stroke, allowing the individual to continue to take discrete samples as it develops. Received: 24 May 2000 / Revised version: 8 May 2001 / Published online: 7 December 2001     

Proprioceptors of the thoracic limbs of Squilla mantis (Crustacea,Stomatopoda)

Summary The distribution and morphology of the internal proprioceptive organs in the thoracic appendages of the stomatopod crustacean, Squilla mantis, are described. Five distinct types of proprioceptor are recognised; connective chordotonal organ, myochordotonal organ, cuticular stress detector, multiterminal stretch receptor and apodeme stretch receptor. The connective chordotonal organs and multiterminal receptors exhibit a wide variety of structural and functional complexity. The stomatopods resemble the decapods in that the basic proprioceptive unit of the thoracic appendages appears to be the connective chordotonal organ, but differs in the higher occurrence of multiterminal stretch receptors. As described for decapods, the pereiopods of stomatopods possess the largest number and greatest variety of proprioceptors, suggesting that locomotion exerts greater selective pressure on proprioceptor development than do the other thoracic limb functions, including the raptorial strike.     

The peripheral and central antennular pathway of the Caribbean stomatopod crustacean Neogonodactylus oerstedii

Although stomatopod crustaceans use their chemical senses in many facets of behavior, little is known about their chemosensory neural pathways, especially in comparison to the better-studied decapod crustaceans. We examined the stomatopod Neogonodactylus oerstedii to determine organizational aspects of peripheral and central neural pathway of antennules, which is a major chemosensory organ. We describe the three flagella of the triramous antennule as the medial, dorsolateral, and ventrolateral flagella. The primary branch point is between the medial flagellum and lateral flagella, and the secondary branch point is at the junction of the dorsolateral and ventrolateral flagella. The antennule bears at least three types of setae, based on their external morphology. Simple setae are present only on the medial flagellum and ventrolateral flagellum, organized as a tuft of 10-15 setae on each flagellar annulus. Aesthetasc setae and asymmetric setae occur only on the distal annuli of the dorsolateral flagellum, with each annulus bearing a row of three aesthetascs and one asymmetric seta. DiI fills of the antennular nerve near the junction of the flagella show that sensory neurons in the antennular flagella project to two neuropils in the ipsilateral midbrain-the olfactory lobe (OL) and lateral antennular neuropil (LAN). The OL is glomerular and has rich serotonergic innervation, a characteristic of the OL in decapods. The LAN is bi-lobed and stratified as it is in decapods. However, the LAN of stomatopods differs from that of decapods in being relatively large and containing extensive serotonergic innervation. The median antennular neuropil of stomatopods has sparse serotonergic innervation, and it is more diffusely organized compared to decapods. No accessory lobes were found in N. oerstedii. Thus, the stomatopod antennular flagella have the same two, highly organized parallel pathways common to decapods-the OL pathway and the LAN pathway.     

Two visual systems in one eyestalk: The unusual optic lobe metamorphosis in the stomatopod Alima pacifica

The compound eyes of adult stomatopod crustaceans have two to six ommatidial rows at the equator, called the midband, that are often specialized for color and polarization vision. Beneath the retina, this midband specialization is represented as enlarged optic lobe lamina cartridges and a hernia‐like expansion in the medulla. We studied how the optic lobe transforms from the larvae, which possess typical crustacean larval compound eyes without a specialized midband, through metamorphosis into the adults with the midband in a two midband‐row species Alima pacifica. Using histological staining, immunolabeling, and 3D reconstruction, we show that the last‐stage stomatopod larvae possess double‐retina eyes, in which the developing adult visual system forms adjacent to, but separate from, the larval visual system. Beneath the two retinas, the optic lobe also contains two sets of optic neuropils, comprising of a larval lamina, medulla, and lobula, as well as an adult lamina, medulla, and lobula. The larval eye and all larval optic neuropils degenerate and disappear approximately a week after metamorphosis. In stomatopods, the unique adult visual system and all optic neuropils develop alongside the larval system in the eyestalk of last‐stage larvae, where two visual systems and two independent visual processing pathways coexist. © 2017 Wiley Periodicals, Inc. Develop Neurobiol 78: 3–14, 2018     

Behavioural evidence for polarisation vision in stomatopods reveals a potential channel for communication.

Polarisation sensitivity (PS) - the ability to detect the orientation of polarised light - occurs in a wide variety of invertebrates [1] [2] and vertebrates [3] [4] [5], many of which are marine species [1]. Of these, the crustacea are particularly well documented in terms of their structural [6] and neural [7] [8] adaptations for PS. The few behavioural studies conducted on crustaceans demonstrate orientation to, or local navigation with, polarised sky patterns [9]. Aside from this, the function of PS in crustaceans, and indeed in most animals, remains obscure. Where PS can be shown to allow perception of polarised light as a 'special sensory quality' [1], separate from intensity or colour, it has been termed polarisation vision (PV). Here, within the remarkable visual system of the stomatopod crustaceans (mantis shrimps) [10], we provide the first demonstration of PV in the crustacea and the first convincing evidence for learning the orientation of polarised light in any animal. Using new polarimetric [11] and photographic methods to examine stomatopods, we found striking patterns of polarisation on their antennae and telson, suggesting that one function of PV in stomatopods may be communication [12]. PV may also be used for tasks such as navigation [5] [9] [13], location of reflective water surfaces [14] and contrast enhancement [1] [15] [16] [17] [18]. It is possible that the stomatopod PV system also contributes to some of these functions.     

Electroantennographic resolution of pulsed pheromone plumes in two species of moths with bipectinate antennae

Trains of 20-ms-duration pulses of pheromone were deliveredat rates of 1–33 Hz to antennal preparations of malesof Bombyx mori and Lymantria dispar, two moth species with bipectinateantennae. Resolution of rapidly pulsed plumes of pheromone wasnot compromised by a complex antennal morphology or by moderatechanges in wind speed (25–50 cm/s). Fourier analysis ofthe electroantennograms resolved the temporal structure of thesignal at frequencies up to 25 Hz for B. mori and up to 5 Hzfor L. dispar. The ability of these sensory structures to identifythe original (unchanged) frequency of the pulse train is particularlynoteworthy because air is slowed by about an order of magnitudeas it passes through bipectinate antennae. Although an unchangingfrequency in slowed airflow may be counterintuitive, this flowpattern, and its effects on odorant patch shape and spacing,is explained from fluid mechanical principles (i.e., the principleof continuity). An unchanging frequency suggests that as deceleratingair passes through a bipectinate antenna, the slowed patchesof odorant are stretched, thinned, and brought closer togetherby the same factor with which they are slowed.     

Tuning of photoreceptor function in three mantis shrimp species that inhabit a range of depths. I. Visual pigments

Visual pigments in many animal species, including stomatopod crustaceans, are adapted to the photic environments inhabited by that species. However, some species occupy a diversity of environments as adults (such as a range of depths in the ocean), and a single set of visual pigments would not be equally adaptive for all habitats in which individuals live. We characterized the visual pigment complements of three species of stomatopod crustaceans, Haptosquilla trispinosa, Gonodactylellus affinis, and Gonodactylopsis spongicola, which are unusual for this group in that each lives at depths from the subtidal to several tens of meters. Using microspectrophotometry, we determined the visual pigments in all classes of main rhabdoms in individuals of each species from shallow or deep habitats. Each species expressed the typical diversity of visual pigments commonly found in stomatopods, but there was little or no evidence of differential expression of visual pigments in animals of any species collected from different depths. Vision in these species, therefore, is not tuned to spectral characteristics of the photic environment by varying the assemblages of visual pigments appearing in their retinas.     

Spectral tuning and the visual ecology of mantis shrimps

The compound eyes of mantis shrimps (stomatopod crustaceans) include an unparalleled diversity of visual pigments and spectral receptor classes in retinas of each species. We compared the visual pigment and spectral receptor classes of 12 species of gonodactyloid stomatopods from a variety of photic environments, from intertidal to deep water (> 50 m), to learn how spectral tuning in the different photoreceptor types is modified within different photic environments. Results show that receptors of the peripheral photoreceptors, those outside the midband which are responsible for standard visual tasks such as spatial vision and motion detection, reveal the well-known pattern of decreasing lambdamax with increasing depth. Receptors of midband rows 5 and 6, which are specialized for polarization vision, are similar in all species, having visual lambdamax-values near 500nm, independent of depth. Finally, the spectral receptors of midband rows 1 to 4 are tuned for maximum coverage of the spectrum of irradiance available in the habitat of each species. The quality of the visual worlds experienced by each species we studied must vary considerably, but all appear to exploit the full capabilities offered by their complex visual systems.     

Stomatopod eye structure and function: a review

Stomatopods (mantis shrimps) possess apposition compound eyes that contain more photoreceptor types than any other animal described. This has been achieved by sub-dividing the eye into three morphologically discrete regions, a mid-band and two laterally placed hemispheres, and within the mid-band, making simple modifications to a commonly encountered crustacean photoreceptor pattern of eight photoreceptors (rhabdomeres) per ommatidium. Optically the eyes are also unusual with the directions of view of the ommatidia of all three eye regions skewed such that over 70% of the eye views a narrow strip in space. In order to scan the world with this strip, the stalked eyes of stomatopods are in almost continual motion. Functionally, the end result is a trinocular eye with monocular range finding capability, a 12-channel colour vision system, a 2-channel linear polarisation vision system and a line scan sampling arrangement that more resembles video cameras and satellite sensors than animal eyes. Not surprisingly, we are still struggling to understand the biological significance of stomatopod vision and attempt few new explanations here. Instead we use this special edition as an opportunity to review and summarise the structural aspects of the stomatopod retina that allow it to be so functionally complex.     

Morphology of stomatopod chemosensory sensilla facilitates fluid sampling

Abstract. Stomatopods, like many marine crustaceans, rely on their sense of smell to detect prey and to find mates (Ache 1982; Zimmer-Faust 1989; Atema & Voigt 1995). In lobsters, crabs, crayfishes, prawns, leptostracans, anaspidans, mysids, amphipods, tanaids, isopods, ostracodes, phyllopods, and cumaceans (Heimann 1984; Hallberg et al. 1992), this detection of odors from distant sources involves specialized chemosensory setae called aesthetascs located on the antennules. The external structure of stomatopod sensilla appears to follow the typical crustacean aesthetasc pattern, but their internal structure has not been previously examined. In this study, we use serial reconstruction from transmission electron microscopy to show that the stomatopod sensilla are aesthetascs. For chemoreception to occur, chemical-containing fluid must be very close to the surface of the aesthetascs, such that odor molecules can diffuse to chemoreceptors on the olfactory receptor neurons inside the aesthetasc. Flicking of stomatopod antennules maximizes fluid penetration near the parts of the sensilla where the cuticle is thinnest, and where the outer dendritic segments are most fully branched with the greatest surface area. Thus, the external and the internal structure of the stomatopod aesthetasc are "matched" to maximize the efficiency of odor arrival at the surface of the olfactory receptor neurons.     

Antipredator defense as a limited resource: unequal predation risk in broods of an insect with maternal care

The allocation of parental investment is a potential sourceof conflict within broods whenever offspring are able obtaindifferential access to the parental resource. Unlike the provisioningof food, parental antipredator behavior is usually considereda resource that benefits all offspring simultaneously. In thethornbug treehopper (Umbonia crassicornis), offspring formaggregations in exposed positions on host-plant stems. Theyare subject to intense predation, and maternal defense is theirprimary means of protection. I examined the distribution ofrisk within these offspring groups, using natural variationin the outcome of more than 500 predation attempts (324 recordedon videotape) by vespid wasps (Pseudopolybia compressa) on18 U. crassicornis aggregations. I found three influences onan individual offspring's risk of predation. The first wasthe presence of a defending female: as expected, offspringwere much more likely to survive contact with a wasp if thefemale was present than if the female had disappeared. Thesecond influence was position relative to other offspring: when wasps were successful in removing an individual, they almostalways removed it from the edge of the group. The third influencewas distance from the female: the closer an offspring was tothe female at the time it was contacted by a wasp, the higherits likelihood of survival. The distribution of risk is determinedlargely by the behavior of defending females and the prey-searchingbehavior of wasps. The nature of risk within these aggregations sets the stage for two forms of sibling rivalry: selfish herdbehavior and competition for access to maternal defense. Italso raises the question of how a parent should allocate defenseamong offspring when it is unable to defend them all simultaneously.     

Comparative experimental taphonomy of eight marine arthropods indicates distinct differences in preservation potential

Global biodiversity patterns in deep time can only be understood fully when the relative preservation potential of each clade is known. The relative preservation potential of marine arthropod clades, a diverse and ecologically important component of modern and past ecosystems, is poorly known. We tackled this issue by carrying out a 205‐day long comprehensive, comparative, taphonomic experiment in a laboratory by scoring up to ten taphonomic characters for multiple specimens of seven crustacean and one chelicerate species (two true crabs, one shrimp, one lobster, one hermit crab, one stomatopod, one barnacle and one horseshoe crab). Although the results are preliminary because we used a single experimental setup and algal growth partially hampered observations, some parts of hermit crabs, stomatopods, swimming crabs and barnacles decayed slowly relative to other parts, implying differential preservation potentials within species, largely consistent with the fossil record of these groups. An inferred parasitic isopod, manifested by a bopyriform swelling within a hermit crab carapace, decayed relatively fast. We found limited variation in the decay rate between conspecifics, and we did not observe size‐related trends in decay rate. Conversely, substantial differences in the decay rate between species were seen after c. 50 days, with shrimps and stomatopods decaying fastest, suggesting a relatively low preservation potential, whereas the lobster, calico crabs, horseshoe crabs and barnacles showed relatively slow decay rates, suggesting a higher preservation potential. These results are supported by two modern and fossil record‐based preservation potential metrics that are significantly correlated to decay rate ranks. Furthermore, we speculate that stemward slippage may not be ubiquitous in marine arthropods. Our results imply that diversity studies of true crabs, lobsters, horseshoe crabs and barnacles are more likely to yield patterns that are closer to their true biodiversity patterns than those for stomatopods, shrimps and hermit crabs.     

中华蜜蜂信息素结合蛋白ASP1 cDNA的克隆及时空表达

信息素结合蛋白（pheromone binding proteins, PBPs）在昆虫信息素的识别、传递和处理过程中具有重要作用。本研究首次克隆了中华蜜蜂Apis cerana cerana的一个PBP基因Ac-ASP1（GenBank序列号为DQ449670）,其预测蛋白具有典型的气味结合蛋白（OBPs）标志（即成熟肽含有6个保守的半胱氨酸）。利用real-time PCR技术对Ac-ASP1在中蜂不同组织和发育历期的时空表达谱进行了鉴定。绝对定量结果显示Ac-ASP1高丰度地表达于工蜂触角（2.07×10⁶ 拷贝数/μg）,而在其他组织（如头、胸、腹、翅及足）中呈低丰度表达（10²拷贝数/μg）; 相对定量结果显示Ac-ASP1在各发育历期如幼虫、蛹以及成虫发育早期（1～6日龄）均有大量表达,而在21日龄前后具有另外一个高丰度表达时期。这些结果可为明确Ac-ASP1在中蜂蜂王信息素信号识别传递过程中的作用提供参考。     

Numerical simulations of odorant detection by biologically inspired sensor arrays

The antennules of many marine crustaceans enable them to rapidly locate sources of odorant in turbulent environmental flows and may provide biological inspiration for engineered plume sampling systems. A substantial gap in knowledge concerns how the physical interaction between a sensing device and the chemical filaments forming a turbulent plume affects odorant detection and filters the information content of the plume. We modeled biological arrays of chemosensory hairs as infinite arrays of odorant flux-detecting cylinders and simulated the fluid flow around and odorant flux into the hair-like sensors as they intercepted a single odorant filament. As array geometry and sampling kinematics were varied, we quantified distortion of the flux time series relative to the spatial shape of the original odorant filament as well as flux metrics that may be important to both organisms and engineered systems attempting to measure plume structure and/or identify chemical composition. The most important predictor of signal distortion is the ratio of sensor diameter to odorant filament width. Achieving high peak properties (e.g. sharpness) of the flux time series and maximizing the total number of odorant molecules detected appear to be mutually exclusive design goals. Sensor arrays inspired specifically by the spiny lobster Panulirus argus and mantis shrimp Gonodactylaceus falcatus introduce little signal distortion but these species' neural systems may not be able to resolve plume structure at the level of individual filaments via temporal properties of the odorant flux. Current chemical sensors are similarly constrained. Our results suggest either that the spatial distribution of flux across the aesthetasc array is utilized by P. argus and G. falcatus, or that such high spatiotemporal resolution is unnecessary for effective plume tracking.     

The relative availabilities of complementary resources affect the feeding preferences of ant colonies

Theory predicts that consumers selecting among complementaryresources will show stronger preferences for items that becomerelatively less available. I tested this hypothesis in a fieldstudy that compared the preferences of ant colonies given simultaneousaccess to experimental foods differing in carbohydrate and proteincontent. In the first part of the study, I examined the effectof nutrient supplementation on colony-level preference in theant Dorymyrmex smithi. Colonies that had received a proteinsolution for 24 h consumed proportionally more carbohydratesthan control colonies that had been given access to water, suggestingthat colonies preferred nutrients when they became relativelyrare. In the second part of the study, I compared colony-levelpreference among eight species of ants that differ in theirrelative access to carbohydrates and protein in the field. Ifound that species with relatively easy access to carbohydratespreferred protein, whereas species with greater access to proteinpreferred carbohydrates. These results suggest that the benefitsof a nutritionally mixed diet coupled with differences in therelative availability of nutrients may explain variation infeeding decisions both within and among ant species.     

Effect of antibody to anisole binding protein on odorant perturbation of Na+-K+ ATPase activity

Odorant perturbation of Na⁺-K⁺ ATPase activity from cow olfactorytissue was strongly affected by ng quantities of antibodiesto anisole binding protein from dog olfactory mucosa. Antibodyprotein (80 ng per ml reaction mixture) prevented odorant perturbationof Na⁺-K⁺ ATPase activity. Antibody effect on odorant perturbationshowed concentration dependence and was active against a numberof different odorous chemicals. Electrophysiological studies(Goldberg et al, 1979) showed that mouse EOG responses due toodorants were inhibited 50% by previous exposure to 0.8 ng antibodies.Thus electrophysiological and biochemical responses showed sensitivityto the antibodies from the anisole binding protein from dogolfactory tissue. It is proposed that NA⁺-K⁺ ATPase may participatein the initiation of nerve signals caused by odorant-enzymecomplex interactions.     

Real-time monitoring of odorant-induced cellular reactions using surface plasmon resonance

Surface plasmon resonance (SPR) is a powerful technique for measuring molecular interaction in real-time. SPR can be used to detect molecule to cell interactions as well as molecule to molecule interactions. In this study, the SPR-based biosensing technique was applied to real-time monitoring of odorant-induced cellular reactions. An olfactory receptor, OR I7, was fused with a rho-tag import sequence at the N-terminus of OR I7, and expressed on the surface of human embryonic kidney (HEK)-293 cells. These cells were then immobilized on a SPR sensor chip. The intensity of the SPR response was linearly dependent on the amount of injected odorant. Among all the aldehyde containing odorants tested, the SPR response was specifically high for octanal, which is the known cognate odorant for the OR I7. This SPR response is believed to have resulted from intracellular signaling triggered by the binding of odorant molecules to the olfactory receptors expressed on the cell surface. This SPR system combined with olfactory receptor-expressed cells provides a new olfactory biosensor system for selective and quantitative detection of volatile compounds.     

Scanning eye movements of the stomatopod crustacean,Neogonodactylus oerstedii,in polarized light fields

ABSTRACT

Stomatopod crustaceans have highly mobile, independently moving compound eyes that are sensitive to both linearly and circularly polarized light. They rotate their eyes to predictable angles when viewing a linearly polarized target, and they scan their eyes frequently to sample the visual field. Angles of scans are roughly perpendicular to the plane of the midband (a set of specialized parallel rows of equatorial ommatidia). We investigated scanning eye movements in one Caribbean stomatopod species (Neogonodactylus oerstedii) in uniform visual fields that were vertically polarized, horizontally polarized, or depolarized. We found that mean eye rotation and scan angles differed significantly among these different treatments. Average scan angles differed by 12°, being more horizontal in a vertically polarized field than in a horizontally polarized one, and also more horizontal in a vertically polarized field than in a depolarized field. Thus, these stomatopods adjusted visual scanning to the polarization of the visual environment.