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.
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.
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).
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.
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.
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