Show Summary Details

Page of

PRINTED FROM the OXFORD RESEARCH ENCYCLOPEDIA, NEUROSCIENCE (neuroscience.oxfordre.com). (c) Oxford University Press USA, 2016. All Rights Reserved. Personal use only; commercial use is strictly prohibited. Please see applicable Privacy Policy and Legal Notice (for details see Privacy Policy).

date: 15 December 2017

Crustacean Olfaction

Summary and Keywords

Olfaction is a chemical sense present not only in mammals, insects, and other terrestrial animals, but also in crustaceans, most of which are aquatic. Crustaceans use olfaction for detecting and responding in appropriate ways to chemicals relevant to most ecological contexts, including: environmental cues indicating quality of food, habitat, and location; interspecies cues indicating presence of predators and competitors; and intraspecific signals indicating social status of conspecifics and presence of possible mating partners. Olfaction is only one of the chemical senses of crustaceans, being distinguished based on anatomical and functional features of the sensory neurons detecting the chemicals and the pathways within the central nervous system that processes this information.

Keywords: chemical senses, chemoreception, Crustacea, lobster, olfactory, receptor neurons

What are Crustaceans?

Crustacea is a vast, disparate, and diverse group of arthropods, composed of nearly 70,000 known extant species and undoubtedly many more undescribed species (Ahyong et al., 2011; Martin & Davis, 2007; Schram, 2012). Not only are crustaceans themselves diverse, but the most specious group of animals, the insects, evolved from aquatic crustaceans. Crustaceans range in size from meter-long to miniscule, and they occupy most of the Earth’s environments from oceans to rivers to marshes to deserts. Crustaceans include familiar animals such as lobsters, crabs, shrimp, crayfish, and barnacles, but also other lesser-known groups such as copepods, amphipods, isopods, phyllocarids, cumaceans, and remipedes. Crustaceans have been studied extensively by scientists of all stripes, including by comparative biologists to understand their adaptations to specific ecological conditions, and by biomedical scientists who use them as model systems for studying issues related to human-related health and disease. Neuroscientists in particular have studied them in detail since the 19th century. Even Sigmund Freud, as a student at the University of Vienna, studied crayfish, in an examination of the neuronal cytoskeleton (Freud, 1882).

What is Olfaction in Crustaceans?

Most crustaceans live in water during most or all of their life, and they detect and respond to chemicals there. But do they “smell” underwater? Do they and other aquatic animals have an olfactory sense? They do, because olfaction is defined by the neural system used, not by the medium in which the animal and its ecologically relevant chemicals, or odorants, are found. One instructive, parallel example is fish, which have the typical vertebrate olfactory system composed of an olfactory organ composed of an olfactory epithelium with olfactory receptor neurons whose axons project via cranial nerve 1, the olfactory nerve, to an olfactory bulb of glomerular organization (Caprio & Derby, 2008). The fact that fish use their olfactory system to detect water soluble rather than volatile odorants does not mean that fish have any less of an olfactory sense than terrestrial vertebrates. An even more instructive example is the frog, which uses its olfactory sense both in water as a tadpole and in air as an adult—the name of this sensory system does not change when the animal transitions from water to land! With crustaceans, it is the same: they have an olfactory sense, yet aquatic crustaceans such as blue crabs and spiny lobsters use it in water; land-living crustaceans such as desert isopods and coconut crabs use it in air; and semi-terrestrial crabs that inhabit both land and water, such as fiddler crabs and ghost crabs, can use it in both media.

Organization of the Olfactory System of Crustaceans

What is the nature of this olfactory sense of crustaceans? Olfaction differs from all other chemical senses of crustaceans in its peripheral and central organization. While there are some differences in the form and complexity of olfactory structures across the diverse clades of crustaceans, there are some fundamental similarities, and these can be amply highlighted using the spiny lobster, a typical decapod crustacean, whose chemical senses have been more thoroughly studied than in any other crustacean species (Derby & Weissburg, 2014; Schmidt & Mellon, 2011).

Peripheral Olfactory System

The peripheral olfactory structures are specialized sensilla called aesthetascs, first identified and named in the 19th century by German scientists. Franz Leydig (Leydig, 1860) provided the first thorough description of specialized sensilla located on the first antennae (antennules) of several crustacean species including amphipods, hermit crabs, and crayfish (Figure 1A). He used the term olfactory cones (Geruchszapfen) for these sensilla and thus was the first to clearly ascribe olfactory function to them. Numerous other descriptions of these sensilla in other crustacean classes followed over the next decades, in which various terms mostly implicating olfactory function were used, including olfactory hairs, olfactory rods, olfactory filaments, Leydig’s tubes, Leydig’s organs. It was only from 1925 onwards that the term aesthetascs (Aesthetasken), which was introduced by Wilhelm Giesbrecht (Giesbrecht, 1892) in a massive monograph on marine copepods, took hold. Unfortunately, Giesbrecht did not provide any etymological explanation for why he chose this Greek word for these structures, and we can only speculate that he had something like “sensitive hair” in mind.

Crustacean OlfactionClick to view larger

Figure 1. Depictions of crustacean aesthetascs and central olfactory pathway in historical comparison: Left—oldest depictions; Right: current depictions. A. Drawings of antennules with aesthetascs from Leydig (1860): (1) hermit crab, (2) crayfish, (3) aquatic isopod. B. Reconstruction of spiny lobster aesthetasc (modified from Grünert & Ache, 1988): AC, auxiliary cell; iDS, inner dendritic segment; oDS, outer dendritic segment; ORN, olfactory receptor neuron. C. Drawing of the olfactory deutocerebrum of the brain of a clawed lobster from Bellonci (1880). Note that the glomerular neuropil marked with Lol (lobo olfattorio) is actually the accessory lobe, the glomerular neuropil marked with He is the olfactory lobe. D. Reconstruction of the olfactory deutocerebrum of the spiny lobster with schematic drawings of the main neuron types (modified from Schmidt & Ache, 1996): A1Nv, antennular nerve; AL, accessory lobe (with CL, central layer; LL, lateral layer; ML, medial layer); LC, lateral soma cluster (contains somata of projection neurons); MC, medial soma cluster (contains somata of local interneurons); MPN, median protocerebral neuropil; OGT, olfactory globular tract; OL, olfactory lobe; PT, protocerebral tract (connecting the central brain with the eyestalk ganglia). Neuron types: (1) ORN afferent axon with uni-glomerular termination; (2) ORN afferent axon with bi-glomerular termination; A, core OL local interneuron; B, rim OL local interneuron; C, OL projection neuron; D, local OL-AL interneuron; E, AL projection neurons.

Aesthetascs have several unique features that together distinguish them from all other chemosensilla of crustaceans (Grünert & Ache, 1988; Hallberg, Johansson, & Elofsson, 1992; Hallberg & Skog, 2011) (Figure 1B). First, they are located on first antennae, also called antennules, specifically on the lateral flagellum of this biramous appendage. Second, the cuticle surrounding the dendrites of the sensory neurons is thin and permeable, which allows odorants to pass from the external environment into a fluid bathing the dendrites. Third, aesthetascs are innervated only by chemoreceptor neurons, not by mechanoreceptor neurons, and thus are unimodal in function. These chemoreceptor neurons are called olfactory receptor neurons, or ORNs. Fourth, each aesthetasc can be innervated by many ORNs, even several hundred in some species such as remipedes and clawed and spiny lobsters (Grünert & Ache, 1988; van der Ham & Felgenhauer, 2006). Fifth, in most cases two outer dendritic segments (modified cilia) arise from each dendrite, and the outer dendritic segments are highly branched. This organization holds for marine, euryhaline, freshwater, and terrestrial species, though there are specializations that are adaptive for life in each environment, including increased resistance to desiccation in terrestrial species (Ghiradella, Case, & Cronshaw, 1968; Gleeson, Wheatly, & Reiber, 1997; Krieger, Sandeman, Sandeman, Hansson, & Harzsch, 2010; Stensmyr, Erland, Hallberg, Wallén, Greenaway, & Hansson, 2005).

The organization of these olfactory sensilla differs fundamentally from the other chemically sensitive sensilla of crustaceans. These non-olfactory sensilla are called “distributed chemoreceptors” because of their broad distribution across the crustacean’s body and appendages, including but not limited to the antennular lateral flagella (Schmidt & Mellon, 2011). Despite having a diversity of forms and functions, distributed chemosensilla have a similar peripheral organization, with features that are distinctive from olfactory sensilla. First, their cuticle is thick and non-permeable, and chemical stimuli enter the sensilla through a terminal pore. Second, they are bimodal, being innervated by both chemoreceptor neurons (CRNs) and mechanoreceptor neurons (MRNs). Third, typically each sensillum is innervated by only a few to about 20 CRNs, in addition to a few MRNs. Fifth, their CRNs have dendrites with only one outer dendritic segment that remains unbranched.

Central Olfactory System

Giuseppe Bellonci (Bellonci, 1880, 1881) was the first to recognize that large neuropils in the deutocerebrum of lobsters and isopods are similar to the olfactory bulbs of vertebrates in being organized into discrete small balls of neuropil called glomeruli. Knowing that the deutocerebrum receives its sensory input from the antennules, Bellonci coined the term olfactory lobes (lobi olfattorï) for these neuropils (Figure 1C). While the identification of olfactory lobes in isopods was valid, it turned out in later studies that the neuropils that Bellonci had described as olfactory lobes in lobsters are actually secondary neuropils that do not receive innervation from the aesthetascs. Since their first correct description by Bertil Hanström (Hanström, 1925), these neuropils are known as accessory lobes. Bellonci and Hanström also identified a neuropil in the eyestalk ganglia as the second stage of the central olfactory pathway of crustaceans. Bellonci (1882) coined the term hemiellipsoid body (corpo emielissoidale) for this neuropil and homologized it with the mushroom body of the insect brain. Hanström (1925) demonstrated that the hemiellipsoid body receives input from projection (output) interneurons of the olfactory lobes whose axons are extremely thin but form the largest axon tract in the crustacean brain, the olfactory globular tract.

Within the central nervous system (CNS), the olfactory pathway is also distinct from the distributed chemoreception pathways in connectivity and organization (Figure 1D). The axons of ORNs project to one pair of neuropils in the deutocerebrum of the central brain, called the olfactory lobes. The olfactory lobes are organized into packages of glia-delineated neuropil called olfactory glomeruli, which are the targets of the ORNs, and also receive neurites of local and output olfactory interneurons (Schachtner, Schmidt, & Homberg, 2005; Schmidt, 2016; Schmidt & Ache, 1992; Schmidt & Mellon, 2011). Such glomerular organization of olfactory centers is a hallmark of many animals, including insects, gastropods, cephalopods, and vertebrates (Chase & Tolloczko, 1993; Eisthen, 2002; Hildebrand & Shepherd, 1997; Leise, 1991; Maynard, 1967). The glomerular organization in olfactory systems of insects and vertebrates has been shown to accommodate an odotopic representation, in which glomeruli have different, even if sometimes overlapping, chemical sensitivities. This is because ORNs that express a specific type of receptor protein, each of which binds to a small subset of all possible odorant molecules, project to one specific glomerulus, and thus confer on it a certain odorant sensitivity. Thus, odor quality is encoded in these olfactory centers as distinct maps of glomerular activity. It may be that other animal clades with glomerular olfactory systems, including crustaceans, use such odotopic representations, but more investigation is necessary to provide experimental support for this. In some groups of decapod crustaceans (spiny lobsters, clawed lobsters, crayfish, mud shrimp), the olfactory lobes are closely associated with large paired neuropils having a distinct glomerular organization, which are called accessory lobes. The accessory lobes do not receive any direct sensory input and seem to be involved in particular aspects of olfactory and multimodal sensory processing. In contrast to the organization of the olfactory lobes and their ORN input, the CRNs of distributed chemosensilla project to paired neuropils associated with the appendages carrying them—the lateral antennular neuropils in the case of the antennules. These neuropils do not have a glomerular substructure, but they are striated perpendicularly to the neuropil-appendage axis. This suggests a somatotopic organization in which the location of distributed chemosensilla on the appendage appears to be represented as a spatial map of the projections of the CRNs and MRNs (Schmidt, 2007; Schmidt, Van Ekeris, & Ache, 1992; Tautz & Müller-Tautz, 1983). Exactly how odor quality is mapped onto these striated neuropils of crustaceans is not known at present. Another interesting feature of the striated neuropils that receive input from distributed chemosensilla is that they house the motor neurons responsible for moving the appendages providing the sensory input. The olfactory lobes, on the other hand, are not contacted by arborizations of motor neurons and therefore do not directly provide any motor output to any appendage.

The projection (output) interneurons from the olfactory lobes (or if present—from the accessory lobes) extend to a second order neuropil, called the hemiellipsoid body. In its position within the central olfactory pathway, the hemiellipsoid body is equivalent to the mushroom body in the insect brain. Like the mushroom body, the hemiellipsoid body is organized into microglomeruli (Mellon, Alones, & Lawrence, 1991), and both neuropils share basic wiring principles supporting the notion that they are homologous structures (Wolff, Harzsch, Hansson, Brown, & Strausfeld, 2012). Although the functional organization of the mushroom body (particularly in the fruit fly Drosophila) has been elucidated in great depth (Aso et al., 2014), at present nothing is known about the functional organization of the hemiellipsoid body.

Function and Physiology of the Olfactory Pathway of Crustaceans

Chemical Cues and Signals as Biologically Important Information for Crustaceans

Like other animals, crustaceans detect, discriminate, and respond to many chemicals in their natural environment. The list of potentially relevant chemicals is long, since organisms and the environments in which they live have thousands of molecules that can carry information. These molecules include relatively unspecialized metabolic products that may indicate the presence and quality of food to generalist consumers (Derby & Sorensen, 2008), as well as molecules of greater specificity that may function in determining the age, sex, and reproductive status of potential mates (Kamio, Schmidt, Germann, Kubanek, & Derby, 2014). They also can indicate predators, symbiotic partners, and pathogens. These molecules can be detected by the chemical senses of crustaceans, and they play roles in allowing crustaceans to meet their biological needs, including acquiring food and shelter, defense from predators, and interacting appropriately with conspecifics including in social interactions and reproduction. Discriminating and identifying ecologically important chemical stimuli can be accomplished by detecting key molecules in mixtures or by discerning small differences in the composition of mixtures, often against a chemical background that is complex and noisy. Beyond determining the identity and concentration of chemicals, crustaceans also have to determine their location in space and time. Such spatio-temporal resolutions enable crustaceans to locate objects of chemical significance in their environment (Ache, Hein, Bobkov, & Principe, 2016; Koehl et al., 2001; Webster & Weissburg, 2001; Zimmer & Zimmer, 2008).

Behavioral Function of Chemosensory Pathways

The chemosensory systems of crustaceans—olfaction and antennular distributed chemoreception—have some similarities and differences in the behaviors that they mediate. In terms of similarities, both can mediate many appetitive feeding behaviors in spiny lobsters (Derby, Steullet, & Horner, 2001), including detecting food-related chemicals, initiating searching behavior, and guiding animals towards the odor source (Horner, Weissburg, & Derby, 2004; Steullet, Dudar, Flavus, Zhou, & Derby, 2001). Both can also mediate antennular flicking (“sniffing”) (Daniel, Fox, & Mehta, 2008) and olfactory learning and discrimination of food chemicals (Steullet, Krützfeldt, Hamidani, Flavus, Ngo, & Derby, 2002). But olfaction and antennular distributed chemoreception differ in other functions. Olfaction solely or principally mediates detection of and response to conspecific chemicals such as sex pheromones, social cues, and alarm cues that function from a distance (Gleeson, 1982; Horner, Schmidt, Edwards, & Derby, 2008a; Horner, Weissburg, & Derby, 2008b; Johnson & Atema, 2005; Kamio, Araki, Nagayama, Matsunaga, & Fusetani, 2005; Kamio, Schmidt, Germann, Kubanek, & Derby, 2014). Antennular distributed chemoreceptors mediates some behaviors that olfaction does not; for example, the asymmetric sensilla, located in the aesthetasc tuft on the antennular lateral flagellum, mediate chemically elicited grooming of the antennules (Schmidt & Derby, 2005; Daniel et al., 2008).

Transduction

The physiology of ORNs has been studied in some detail, including olfactory transduction pathways, mainly in spiny lobsters. A major class of olfactory receptor proteins across crustaceans is the ionotropic receptors, or IRs. The IRs diversified from ionotropic glutamate receptors in ancient protostomes and are found in all protostome clades, but not in deuterostomes (Benton, 2015; Benton, Vannice, Gomez-Diaz, & Vosshall, 2009; Croset et al. 2010). They have been identified in all examined crustaceans (Corey, Bobkov, Ukhanov, & Ache, 2013; Croset et al. 2010; Derby, Kozma, Senatore, & Schmidt, 2016; Groh, Vogel, Stensmyr, Grosse-Wilde, & Hansson, 2014; Groh-Lunow, Getahun, Grosse-Wilde, & Hansson, 2015; Rytz, Croset, & Benton, 2013). Classes of receptors that are present in other animals—the GR/OR family of ionotropic seven-transmembrane receptors that are common in insects (Robertson, 2015; Saina et al., 2015), and the seven-transmembrane G-protein coupled receptors mediating chemoreception including olfaction in vertebrates (Churcher & Taylor, 2010; Niimura, 2012), have not been found in crustaceans, with the exception of GRs in the water flea Daphnia pulex (Peñalva-Arana, Lynch, & Robertson, 2009). Receptor binding studies using dendritic membrane preparations from isolated aesthetascs with radiolabeled chemicals have characterized high- and low-affinity receptor proteins that bind bioactive odorants such as taurine, adenosine-5′-monophosphate, L-glutamate, and L-alanine (Gentilcore & Derby, 1998; Michel, Trapido-Rosenthal, Chao, & Wachowiak, 1993; Olson & Derby, 1995; Olson, Trapido-Rosenthal, & Derby, 1992). The response specificities of ORNs are diverse, as revealed by patch-clamping (Doolin & Ache, 2005; Michel & Ache, 1994; Michel et al., 1993; Simon & Derby, 1995). Most ORNs can be excited as well as inhibited by different sets of odorants. Based on these molecular, biochemical, and physiological studies, we expect dozens of olfactory receptor proteins in spiny lobsters. There is physiological evidence that spiny lobster ORNs use two G-protein mediated transduction cascades, involving the second messengers cAMP and inositol phosphates, with the former mediating inhibition and the latter mediating excitation (Boekhoff, Michel, Breer, & Ache, 1994; Hatt & Ache, 1994; McClintock, Ache, & Derby, 2006). But given that the receptor proteins seem to be IRs and hence would be directly gated by odorant binding, how G-protein cascades are involved in olfactory transduction of crustaceans remains to be explained.

Coding

Once transduction is effected, key defining features of chemical stimuli need to be coded, including chemical quality, intensity, and location in space and time. Neural coding in crustacean chemoreception has been studied by comparing perceptual abilities of animals with information available in different neural representations. Crustacean chemosensory systems appear to encode the chemical quality of food-related stimuli using a distributed code, also called a population or across-neuron pattern code (Atema & Voigt, 1995; Derby, 2000). For example, distributed codes for chemical mixtures representing the tissues of crab, shrimp, mullet, and oyster are different from each other, and these differences in codes are correlated with the compositional differences in these mixtures. Stimulus intensity, instead, is encoded by the intensity rather than pattern of the population response. Behavioral studies show that spiny lobsters perceive as most similar mixtures with the most similar composition and most similar distributed codes (Derby, 2000), suggesting that crustaceans discriminate the quality of natural, complex chemical stimuli based on distributed codes. The spatial and temporal properties of chemical stimuli can inform crustaceans about the location of the source of the chemicals (Koehl et al., 2001; Webster & Weissburg, 2001; Zimmer & Zimmer, 2008). The ability of and speed whereby receptor neurons adapt and disadapt to chemical stimuli, and their ability to follow high frequency pulses of chemicals, will determine their ability to resolve spatiotemporal features of chemicals in their environment (Borroni & Atema, 1988; Gomez & Atema, 1996a, 1996b). In addition to these features of cells, there is a population of ORNs in spiny lobsters that are spontaneous rhythmic bursters and whose activity becomes entrained to presentation of chemicals (Bobkov & Ache, 2007). Modeling studies suggest that these bursting ORNs may have the capacity to encode temporal properties of intermittent chemical signals and that this may help animals locate the source of chemicals in environments that simulate naturally turbulent conditions (Ache, Hein, Bobkov, & Principe, 2016; Park, Bobkov, Ache, & Príncipe, 2014; Park, Hein, Bobkov, Reidenbach, Ache, & Príncipe, 2016).

Neurogenesis in the Olfactory Pathway of Adult Crustaceans

The olfactory pathway of decapod crustaceans parallels that of vertebrates including mammals in having continuous adult neurogenesis, that is the addition of new neurons to the peripheral and central nervous systems of adult animals. In the peripheral olfactory pathway of adult crustaceans, with each molt, new ORNs and their aesthetasc sensilla are generated in a proliferation zone that is proximal to the functionally mature aesthetascs, and old ORNs are lost distally (Harrison, Cate, Swanson, & Derby, 2001; Steullet, Cate, & Derby, 2000). This generates a slow turnover of ORNs and results in a longitudinal age gradient along the aesthetasc array. In the central olfactory pathway of adult crustaceans, new interneurons are generated in small proliferation zones located deep within the clusters of somata of mature interneurons (Schmidt, 2014; Sullivan, Benton, Sandeman, & Beltz, 2007a). All decapod species analyzed have adult neurogenesis in the olfactory deutocerebrum, which includes the first synaptic relay of the central olfactory pathway, the olfactory lobe. In the olfactory deutocerebrum, each proliferation zone is associated with one large adult neuroblast, likely acting as an asymmetrically dividing neural stem cell (Schmidt, 2014; Schmidt & Derby, 2011). Each adult neuroblast is embedded in a presumptive neurogenic niche composed of small bipolar cells whose identity is currently controversial (glial vs. ectodermal) (Schmidt, 2014; Schmidt & Derby, 2011; Sullivan, Sandeman, Benton, & Beltz, 2007b). Overall, adult neurogenesis in the olfactory deutocerebrum of decapods parallels adult neurogenesis in the brain of mammals and insects in being based on the same type of neuronal stem cell as is embryonic neurogenesis (Schmidt, 2014).

What We Don’t Know but Should About Crustacean Olfaction

Much still remains to be learned about the behaviors controlled by olfaction and the organization of the neural pathways mediating them. For example, how is information about odors, be they from food, predators, conspecific social or sexual partners, symbiotic partners, or other sources, be represented peripherally in the ORNs of the aesthetasc sensilla, and how is this peripheral information mapped in the brain’s olfactory lobes? That is, what is the olfactory wiring logic? Little is known about the molecular identity of most biologically relevant odors, including pheromones and other intraspecific cues, and even food odors are not completely characterized. This is important not only in understanding the chemical ecology of crustaceans but also in providing identified molecules to be used as probes in understanding the olfactory wiring logic. Modern molecular biological techniques, including genomic, transcriptomic, and proteomic approaches, can now be applied to crustaceans, making it possible to perform descriptive and experimental studies to understand the molecular organization of crustacean olfaction, including identifying the receptor molecules and transduction pathways that define and distinguish ORNs from the other chemoreceptor neurons. Clearly, while much has been learned about crustacean olfaction over the last 150 years, much remains to be discovered.

References

Ache, B. W., Hein, A. M., Bobkov, Y. V., & Principe, J. C. (2016). Smelling time: a neural basis for olfactory scene analysis. Trends in Neurosciences, 39, 649–655.Find this resource:

Ahyong, S. T., Lowry, J. K., Alonso, M., Bamber, R. N., Boxshall, G. A., Castro, P., et al. (2011). Subphylum Crustacea Brünnich, 1772. In Z.-Q. Zhang (Ed.), Animal biodiversity: An outline of higher-level classification and survey of taxonomic richness (pp. 165–191). Zootaxa 3148. Auckland, New Zealand: Magnolia Press.Find this resource:

Aso, Y., Hattori, D., Yu, Y., Johnston, R. M., Iyer, N. A., Ngo, T-T. B., et al. (2014). The neuronal architecture of the mushroom body provides a logic for associative learning. eLife, 3.Find this resource:

Atema, J., & Voigt, R. (1995). Behavior and sensory biology. In J. R. Factor (Ed.), Biology of the lobster, Homarus americanus (pp. 331–348). San Diego, CA: Academic Press.Find this resource:

Bellonci, G. (1880). Sui lobi olfattorï del Nephrops norwegicus. Memorie della Accademia delle Scienze dell’Istituto di Bologna.Serie, 4(1), 429–431.Find this resource:

Bellonci, G. (1881). Sistema nervoso e organi dei sensi dello Sphaeroma serratum. Atti della Reale Accademia dei Lincei. Serie, 3(10), 91–103.Find this resource:

Bellonci, G. (1882). Nuove ricerche sulla struttura del ganglio ottico della Squilla mantis. Memorie della Accademia delle Scienze dell’Istituto di Bologna Serie, 4(3), 419–426.Find this resource:

Benton, R. (2015). Multigene family evolution: Perspectives from insect chemoreceptors. Trends in Ecology & Evolution, 30, 590–600.Find this resource:

Benton, R., Vannice, K. S., Gomez-Diaz, C., & Vosshall, L. B. (2009). Variant ionotropic glutamate receptors as chemosensory receptors in Drosophila. Cell, 136, 149–162.Find this resource:

Bobkov, Y. V., & Ache, B. W. (2007). Intrinsically bursting olfactory receptor neurons. Journal of Neurophysiology, 97, 1052–1057.Find this resource:

Boekhoff, I., Michel, W. C., Breer, H., & Ache, B. W. (1994). Single odors differentially stimulate dual second messenger pathways in lobster olfactory receptor cells. Journal of Neuroscience, 14, 3304–3309.Find this resource:

Borroni, P. F., & Atema, J. (1988). Adaptation in chemoreceptor cells: I. Self-adapting backgrounds determine threshold and cause parallel shift of response function. Journal of Comparative Physiology A, 164, 67–74.Find this resource:

Caprio, J., & Derby, C. D. (2008). Aquatic animal models in the study of chemoreception. In S. Firestein & G. K. Beauchamp (Eds.), Olfaction & taste: Vol. 4.The senses (pp. 97–134). San Diego, CA: Academic Press.Find this resource:

Chase, R., & Tolloczko, B. (1993). Tracing neural pathways in snail olfaction: From the tip of the tentacles to the brain and beyond. Microscopy Research and Technique, 24, 214–230.Find this resource:

Churcher, A. M., & Taylor, J. S. (2010). The antiquity of chordate odorant receptors is revealed by the discovery of orthologs in the cnidarian Nematostella vectensis. Genome Biology and Evolution, 3, 36–43.Find this resource:

Corey, E. A., Bobkov, Y., Ukhanov, K., & Ache, B. W. (2013). Ionotropic crustacean olfactory receptors. PLoS ONE, 8.Find this resource:

Croset, V., Rytz, R., Cummins, S. F., Budd, A., Brawand, D., Kaessmann, H., et al. (2010). Ancient protosome origin of chemosensory ionotropic glutamate receptors and the evolution of insect taste and olfaction. PLoS Genetics, 6.Find this resource:

Daniel, P. C., Fox, M., & Mehta, S. (2008). Identification of chemosensory sensilla mediating antennular flicking behavior in Panulirus argus, the Caribbean spiny lobster. Biological Bulletin, 215, 24–33.Find this resource:

Derby, C. D. (2000). Learning from spiny lobsters about chemosensory coding of mixtures. Physiology & Behavior, 69, 203–209.Find this resource:

Derby, C. D., Kozma, M. T., Senatore, A., & Schmidt, M. (2016). Molecular mechanisms of reception and perireception in crustacean chemoreception: A comparative review. Chemical Senses, 41, 381–398.Find this resource:

Derby, C. D., & Sorensen, P. W. (2008). Neural processing, perception, and behavioral responses to natural chemical stimuli by fish and crustaceans. Journal of Chemical Ecology, 34, 898–914.Find this resource:

Derby, C. D., Steullet, P., & Horner, A. J. (2001). The sensory basis to feeding behavior in the Caribbean spiny lobster Panulirus argus. Marine and Freshwater Research, 52, 1339–1350.Find this resource:

Derby, C. D., & Weissburg, M. J. (2014). The chemical senses and chemosensory ecology of crustaceans. In C. Derby & M. Thiel (Eds.), Nervous systems & control of behavior: Vol. 3. The Natural history of the crustacea (pp. 263–292). New York: Oxford University Press.Find this resource:

Doolin, R. E., & Ache, B. W. (2005). Specificity of odorant-evoked inhibition in lobster olfactory receptor neurons. Chemical Senses, 30, 105–110.Find this resource:

Eisthen, H. L. (2002). Why are olfactory systems of different animals so similar? Brain Behavior and Evolution, 59, 273–293.Find this resource:

Freud, S. (1882). Über den Bau der Nervenfasern und Nervenzellen beim Flusskrebs. Sitzungsberichte der Kaiserlichen Akademie der Wissenschaften in Wien, 85, 9–46.Find this resource:

Gentilcore, L. R., & Derby, C. D. (1998). Complex binding interactions between multicomponent mixtures and odorant receptors in the olfactory organ of the Caribbean spiny lobster Panulirus argus. Chemical Senses, 23, 269–281.Find this resource:

Ghiradella, H. T., Case, J. F., & Cronshaw, J. (1968). Structure of aesthetascs in select marine and terrestrial decapods: Chemoreceptor morphology and environment. American Zoologist, 8, 603–621.Find this resource:

Giesbrecht, W. (1892). Systematik und Faunistik der pelagischen Copepoden des Golfes von Neapel und der angrenzenden Meeres-Abschnitte. Berlin: Verlag R. Friedländer & Sohn.Find this resource:

Gleeson, R. A. (1982). Morphological and behavioral identification of sensory structures mediating pheromone reception in the blue crab, Callinectes sapidus. Biological Bulletin, 163, 162–171.Find this resource:

Gleeson, R. A., Wheatly, M. G., & Reiber, C. L. (1997). Perireceptor mechanisms sustaining olfaction at low salinities: Insight from the euryhaline blue crab Callinectes sapidus. Journal of Experimental Biology, 200, 445–456.Find this resource:

Gomez, G., & Atema, J. (1996a). Temporal resolution in olfaction: Stimulus integration time of lobster chemoreceptor cells. Journal of Experimental Biology, 199, 1771–1779.Find this resource:

Gomez, G., & Atema, J. (1996b). Temporal resolution in olfaction: II. Time course of recovery from adaptation in lobster chemoreceptor cells. Journal of Neurophysiology, 76, 1340–1343.Find this resource:

Groh, K. C., Vogel, H., Stensmyr, M. C., Grosse-Wilde, E., & Hansson, B. S. (2014). The hermit crab’s nose: Antennal transcriptomics. Frontiers in Neuroscience, 7, 266.Find this resource:

Groh-Lunow, K. C., Getahun, M. N., Grosse-Wilde, E., & Hansson, B. S. (2015). Expression of ionotropic receptors in terrestrial hermit crab’s olfactory sensory neurons. Frontiers in Neuroscience, 8, 448.Find this resource:

Grünert, U., & Ache, B. W. (1988). Ultrastructure of the aesthetasc (olfactory) sensilla of the spiny lobster, Panulirus argus. Cell and Tissue Research, 25, 95–103.Find this resource:

Hallberg, E., Johansson, K. U. I., & Elofsson, R. (1992). The aesthetasc concept: Structural variations of putative olfactory receptor cell complexes in Crustacea. Microscopy Research and Technique, 22, 325–335.Find this resource:

Hallberg, E., & Skog, M. (2011). Chemosensory sensilla in crustaceans. In T. Breithaupt & M. Thiel (Eds.), Chemical Communication in Crustaceans (pp. 103–121). London: Springer Science.Find this resource:

Hanström, B. (1925). The olfactory centers in crustaceans. Journal of Comparative Neurology, 38, 221–250.Find this resource:

Harrison, P. J. H., Cate, H. S., Swanson, E. S., & Derby, C. D. (2001). Postembryonic proliferation in the spiny lobster antennular epithelium: Rate of genesis of olfactory receptor neurons is dependent on molt stage. Journal of Neurobiology, 47, 51–66.Find this resource:

Hatt, H., & Ache, B. W. (1994). Cyclic nucleotide- and inositol phosphate-gated ion channels in lobster olfactory receptor neurons. Proceedings of the National Academy of Sciences, USA, 91, 6264–6268.Find this resource:

Hildebrand, J. G., & Shepherd, G. M. (1997). Mechanisms of olfactory discrimination: Converging evidence for common principles across phyla. Annual Review of Neuroscience, 20, 595–631.Find this resource:

Horner, A. J., Weissburg, M. J., & Derby, C. D. (2004). Dual antennular chemosensory pathways can mediate orientation by Caribbean spiny lobsters in naturalistic flow conditions. Journal of Experimental Biology, 207, 3785–3796.Find this resource:

Horner, A. J., Schmidt, M., Edwards, D. H., & Derby, C. D. (2008a). Role of the olfactory pathway in agonistic behavior of crayfish Procambarus clarkii. Invertebrate Neuroscience, 8, 11–18.Find this resource:

Horner, A. J., Weissburg, M. J., & Derby, C. D. (2008b). The olfactory pathway mediates sheltering behavior of Caribbean spiny lobsters, Panulirus argus, to conspecific urine signals. Journal of Comparative Physiology A, 194, 243–253.Find this resource:

Johnson, M. E., & Atema, J. (2005). The olfactory pathway for individual recognition in the American lobster, Homarus americanus. Journal of Experimental Biology, 208, 2865–2872.Find this resource:

Kamio, M., Araki, M., Nagayama, T., Matsunaga, S., & Fusetani, N. (2005). Behavioral and electrophysiological experiments suggest that the antennular outer flagellum is the site of pheromone reception in the male helmet crab Telmessus cheiragonus. Biological Bulletin, 208, 12–19.Find this resource:

Kamio, M., Schmidt, M., Germann, M. W., Kubanek, J., & Derby, C. D. (2014). The smell of moulting: N-acetylglucosamino-1,5-lactone is a moulting biomarker and candidate courtship signal in the urine of the blue crab, Callinectes sapidus. Journal of Experimental Biology, 217, 1286–1296.Find this resource:

Koehl, M. A. R., Koseff, J. R., Crimaldi, J. P., McCay, M. G., Cooper, T., Wiley, M. B., et al. (2001). Lobster sniffing: Antennule design and hydrodynamic filtering of information in an odor plume. Science, 294, 1948–1951.Find this resource:

Krieger, J., Sandeman, R. E., Sandeman, D. C., Hansson, B. S., & Harzsch, S. (2010). Brain architecture of the largest living land arthropod, the giant robber crab Birgus latro (Crustacea, Anomura, Coenobitidae): Evidence for a prominent central olfactory pathway? Frontiers in Zoology, 10, 25.Find this resource:

Leise, E. M. (1991). Evolutionary trends in invertebrate ganglionic structure. Seminars in Neuroscience, 3, 369–377.Find this resource:

Leydig, F. (1860). Über Geruchs- und Gehörorgane der Krebse und Insekten. Archiv für Anatomie, Physiologie und wissenschaftliche Medicin, 3, 265–314.Find this resource:

Martin, J. W., & Davis, G. E. (2007). Historical trends in crustacean systematics. Crustaceana, 79, 1347–1368.Find this resource:

Maynard, D. M. (1967). Organization of central ganglia. In C. A. G. Wiersma (Ed.), Invertebrate nervous systems: Their significance for mammalian neurophysiology (pp. 231–255). Chicago: University of Chicago Press.Find this resource:

McClintock, T. S., Ache, B. W., & Derby, C. D. (2006). Lobster olfactory genomics. Integrative and Comparative Biology, 46, 940–947.Find this resource:

Mellon, D., Jr., Alones, V., & Lawrence, M. D. (1991). Fine structure of olfactory-globular tract axon terminals in the crayfish brain. Presented to the 21st Annual Meeting, New Orleans, LA. Society for Neuroscience Abstracts, 17, 640.Find this resource:

Michel, W. C., & Ache, B. W. (1994). Odor-evoked inhibition in primary olfactory receptor neurons. Chemical Senses, 19, 11–24.Find this resource:

Michel, W. C., McClintock, T. S., & Ache, B. W. (1991). Inhibition of lobster olfactory receptor cells by an odor-activated potassium conductance. Journal of Neurophysiology, 65, 446–453.Find this resource:

Michel, W. C., Trapido-Rosenthal, H. G., Chao, E. T., & Wachowiak, M. (1993). Stereoselective detection of amino acids by lobster olfactory receptor neurons. Journal of Comparative Physiology A, 171, 705–712.Find this resource:

Niimura, Y. (2012). Olfactory receptor multigene family in vertebrates: From the viewpoint of evolutionary genomics. Current Genomics, 13, 103–114.Find this resource:

Olson, K. S., & Derby, C. D. (1995). Inhibition of taurine and 5′AMP olfactory receptor sites of the spiny lobster Panulirus argus by odorant compounds and mixtures. Journal of Comparative Physiology A, 176, 527–540.Find this resource:

Olson, K. S., Trapido-Rosenthal H. G., & Derby, C. D. (1992). Biochemical characterization of independent olfactory receptor sites for 5′-AMP and taurine in the spiny lobster. Brain Research, 583, 262–270.Find this resource:

Park, I. J., Hein, A. M., Bobkov, Y. V., Reidenbach, M. A., Ache, B. W., & Príncipe, J. C. (2016). Neurally encoding time for olfactory navigation. PLoS Computational Biology, 12, e1004682.Find this resource:

Park, I. M., Bobkov, Y. V., Ache, B. W., & Príncipe, J. C. (2014). Intermittency coding in the primary olfactory system: A neural substrate for olfactory scene analysis. Journal of Neuroscience, 34, 941–952.Find this resource:

Peñalva-Arana, D.C., Lynch, M., & Robertson, H. M. (2009). The chemoreceptor genes of the waterflea Daphnia pulex: Many Grs but no Ors. BMC Evolutionary Biology, 9, 79.Find this resource:

Robertson, H. M. (2015). The insect chemoreceptor superfamily is ancient in animals. Chemical Senses, 40, 609–614.Find this resource:

Rytz, R., Croset, V., & Benton, R. (2013). Ionotropic receptors (IRs): Chemosensory ionotropic glutamate receptors in Drosophila and beyond. Insect Biochemistry and Molecular Biology, 43, 888–897.Find this resource:

Saina, M., Busengdal, H., Sinigaglia, C., Petrone, L., Oliveri, P., Rentzsch, F., et al. (2015). A cnidarian homologue of an insect gustatory receptor functions in developmental body patterning. Nature Communications, 6, 6243.Find this resource:

Schachtner, J., Schmidt, M., & Homberg, U. (2005). Organization and evolutionary trends of primary olfactory brain centers in Tetraconata (Crustacea+Hexapoda). Arthropod Structure and Development, 34, 257–299.Find this resource:

Schmidt, M. (2007). The olfactory pathway of decapod crustaceans: An invertebrate model for life-long neurogenesis. Chemical Senses, 32, 365–384.Find this resource:

Schmidt, M. (2014). Adult neurogenesis. In C. Derby & M. Thiel (Eds.), Nervous systems & control of Behavior: Vol. 3. The natural history of the crustacea (pp. 175–205). New York: Oxford University Press.Find this resource:

Schmidt, M. (2016). Malacostraca. In A. Schmidt-Rhaesa, S. Harzsch, & G. Purschke (Eds.), Structure and evolution of invertebrate nervous systems (pp. 529–582). New York: Oxford University Press.Find this resource:

Schmidt, M., & Ache, B.W. (1992). Antennular projections to the midbrain of the spiny lobster. II. Sensory innervation of the olfactory lobe. Journal of Comparative Neurology, 318, 291–303.Find this resource:

Schmidt, M., & Ache, B. W. (1996). Processing of antennular input in the brain of the spiny lobster, Panulirus argus: II. The olfactory pathway. Journal of Comparative Physiology A, 178, 605–628.Find this resource:

Schmidt, M., & Derby, C. D. (2005). Non-olfactory chemoreceptors in asymmetric setae activate antennular grooming behavior in the Caribbean spiny lobster, Panulirus argus. Journal of Experimental Biology, 208, 233–248.Find this resource:

Schmidt, M., & Derby, C. D. (2011). Cytoarchitecture and ultrastructure of neural stem cell niches and neurogenic complexes maintaining adult neurogenesis in the olfactory midbrain of spiny lobsters, Panulirus argus. Journal of Comparative Neurology, 519, 2283–2319.Find this resource:

Schmidt, M., & Mellon, D., Jr. (2011). Neuronal processing of chemical information in crustaceans. In T. Breithaupt & M. Thiel (Eds.), Chemical communication in crustaceans (pp. 123–147). New York: Springer.Find this resource:

Schmidt, M., Van Ekeris, L., & Ache, B. W. (1992). Antennular projections to the midbrain of the spiny lobster. I. Sensory innervation of the lateral and medial antennular neuropils. Journal of Comparative Neurology, 318, 277–290.Find this resource:

Schram, F. S. (2012). Comments on crustacean biodiversity and disparity of body forms. In L. Watling & M. Thiel (Eds.), Functional morphology and diversity: Vol. 1. The natural history of crustacea (pp. 1–33). New York: Oxford University Press.Find this resource:

Simon, T. W., & Derby, C. D. (1995). Mixture suppression without inhibition for binary mixtures from whole cell patch clamp studies of in situ olfactory receptor neurons of the spiny lobster. Brain Research, 678, 213–224.Find this resource:

Stensmyr, M. C., Erland, S., Hallberg, E., Wallén, R., Greenaway, P., & Hansson, B. S. (2005). Insect-like olfactory adaptations in the terrestrial giant robber crab. Current Biology, 15, 116–121.Find this resource:

Steullet, P., Cate, H. S., & Derby, C. D. (2000). A spatiotemporal wave of turnover and functional maturation of olfactory receptor neurons in the spiny lobster Panulirus argus. Journal of Neuroscience, 20, 3282–3294.Find this resource:

Steullet, P., Dudar, O., Flavus, T., Zhou, M., & Derby, C. D. (2001). Selective ablation of antennular sensilla on the Caribbean spiny lobster Panulirus argus suggests that dual antennular chemosensory pathways mediate odorant activation of searching and localization of food. Journal of Experimental Biology, 204, 4259–4269.Find this resource:

Steullet, P., Krützfeldt, D. R., Hamidani, G., Flavus, T., Ngo, V., & Derby C. D. (2002). Dual parallel antennular chemosensory pathways mediate odor-associative learning and odor discrimination in the Caribbean spiny lobster Panulirus argus. Journal of Experimental Biology, 205, 851–867.Find this resource:

Sullivan, J. M., Benton, J. L., Sandeman, D. C., & Beltz, B. S. (2007a). Adult neurogenesis: A common strategy across diverse species. Journal of Comparative Neurology, 500, 574–584.Find this resource:

Sullivan, J. M., Sandeman, D. C., Benton, J. L., & Beltz, B. S. (2007b). Adult neurogenesis and cell cycle regulation in the crustacean olfactory pathway: From glial precursors to differentiated neurons. Journal of Molecular Histology, 38, 527–542.Find this resource:

Tautz, J., & Müller-Tautz, R. (1983). Antennal neuropile in the brain of the crayfish: Morphology of neurons. Journal of Comparative Neurology, 218, 415–425.Find this resource:

van der Ham, J. L., & Felgenhauer, B. E. (2006). Ultrastructure of the peduncular aesthetascs of Speleonectes tanumekes (Crustacea, Remipedia) in comparison with crustaceans from stressful environments. Invertebrate Biology, 125, 256–264.Find this resource:

Webster, D. R., & Weissburg, M. J. (2001). Chemosensory guidance cues in a turbulent odor plume. Limnology and Oceanography, 46, 1048–1053.Find this resource:

Wolff, G., Harzsch, S., Hansson, B. S., Brown, S., & Strausfeld, N. (2012). Neuronal organization of the hemiellipsoid body of the land hermit crab, Coenobita clypeatus: Correspondence with the mushroom body ground pattern. Journal of Comparative Neurology, 520, 2824–2846.Find this resource:

Zimmer, R. K., & Zimmer, C. A. (2008). Dynamic scaling in chemical ecology. Journal of Chemical Ecology, 34, 822–836.Find this resource: