Abstract
Brachyura (true crabs) largely rely on chemical cues and signals to navigate the turbulent benthic boundary layer (BBL), which is largely constituted by high-resolution plumes. A dual-chemosensory pathway employs this navigation: far-field olfaction and near-field distributed chemoreception. Both of these make up the peripheral system by capturing fine-scale spatio-temporal cues and signals. However, there still lies a fundamental disconnect between the mechanics of peripheral input and central neural processing.
This literature review is comprised of the current understanding of chemosensory neuroethology in benthic-thriving Brachyurans, concentrating on three major research gaps. Initially, the mechanical function and the neural processes of behaviors like “the sniff” and plume navigation are poorly understood. It is also unknown if the CNS decodes and interprets the mentioned fine-scale spatiotemporal odor plumes or if high-resolution input is gone before reaching the olfactory lobe. Lastly, it is understood that Brachyurans utilize a bimodal system, comprised of an olfactory and chemosensory system; the question that remains is the mechanism at which information is combined from far-field olfaction and near-field chemoreception to synthesize a unified decision. This literature review aims to compile current knowledge on these major research gaps and provide possible methodologies to bridge the neural-physical divide in benthic Brachyura.
Highlights
- Benthic Brachyura (true crabs) depend extensively on chemical cues and signals to navigate the turbulent benthic boundary layer (BBL), where high-resolution plumes are often captured and processed.
- Brachyurans and numerous other decapod crustaceans possess a bimodal peripheral sensory system, integrating both a chemoreceptive system and an olfactory system.
- The molecular pathway that allows brachyurans to detect chemical cues and signals is primarily mediated by the Ionotropic Receptor (IR) family.
- Quantification and visualization of chemical concentration and composition can be achieved by utilizing Planar Laser-Induced Fluorescence (PLIF) [44]. To monitor neural activity, central neural techniques such as calcium imaging or voltage-sensitive dye imaging must be coupled.
Brachyuran reliance on chemoreception and systems
The chemosensory world of many crustaceans influences their survival through their ability to interact with conspecifics [17], evade predators [64], forage for resources [36], and reproduce [23]. In benthic crustaceans, specifically true crabs (Brachyura), chemical cues, signals, and stimuli are moved by dynamic water movements [4],[20]. These water movements generate odor plumes, which are highly complex in chemical nature, nonuniform, and diffuse into clouds shortly after they’re generated [31,[71]. The interaction between odor plumes and the benthic boundary layer (the link between the benthos and the water column) often determines the chemosensor’s spatiotemporal viability in relation to the Brachyuran [20],[54]. Cues and signals are rarely comprised of a single element, therefore, Brachyurans must be able to obtain meaningful information via the peripheral sensory system from an often heterogeneous and turbulent environment [19],[65].
Brachyurans and many other decapod crustaceans possess a dual-chemosensory apparatus within their peripheral sensory system: a distributed chemoreceptive system and an olfactory system [19]. Each pathway has a separate mechanism of collection and integration [40]. The distributed chemoreceptive system is highly dispersed across a Brachyuran’s anatomy, detecting near-field stimuli [41]. The function of this system aids in the localization of stimuli and quality evaluation, but only at a high threshold (Ledesma & Monteclaro 2017); stimuli must be, relative to the brachyuran or captured in high concentrations [51]. It is bimodal, as chemoreceptor neurons (CRNs) and mechanoreceptor neurons (MRNs) innervate the sensilla (sensory hairs) that make up the distributed chemosensory system [60]. CRNs within the distributed system project to the Subesophageal Ganglion (SOG) [40]. MRNs project directly into the segmental thoracic ganglia, which are extensive sensory and motor neuropils [18]. Bimodal sensilla are found on the dactyls of the pereiopods and utilized in contact chemoreception [20]. The mouthparts are also used in the distributed system and covered in sensilla, specifically the maxillipeds and mandibles [10],[51]. Other body surfaces, including the first and second antennules and oesophagus, possess significantly fewer bimodal sensilla and are studied less extensively [10].
The olfactory system is comprised of densely packed aesthetascs positioned on the lateral flagella, found only on the first pair of antennae [26],[40]. These are distinguished by their thin walls, and are innervated by unimodal olfactory receptor neurons (ORNs), that can detect the slightest chemical plumes [7]. Central projections of the ORNs target the Olfactory Lobe (OL) in the brachyuran brain [41]. The OL are organized into glomeruli, which are areas of high synaptic activity [7],[19]. These act as the center for processing olfactory information [7]. This occurs within the deutocerebrum, with the output pathway provided by Projection Neurons (PNs) [18]. Cluster 10 (CL10) houses the somata (cell bodies) of the PNs and extends to the Olfactory Globular Tract (OGT) [40] (Hollmann et al. 2021). The OGT is divided into two sections and projects to the protocerebral neuropils in each eyestalk [41], which is where hemiellipsoid bodies are located [74].
Gaps in neuroethology and climate stress
Research in the past century has focused on identifying the crustacean peripheral mechanics involved in proprioceptive systems and molecular-level organization, but a disconnect exists in Brachyuran neuroethology (Thiel & Breithaupt, 2014). Current research indicates that several behavioral responses, such as reproductive behavior in Carcinus maenas, are involved with the Central Nervous System (CNS) [23]; however, the precise mechanism by which this central integration decodes and utilizes high-resolution information remains unrecognized [20],[40]. This neural-physical divide represents a critical research gap within the field [20]. Additionally, there is minimal research identifying the chemical compounds that comprise stimuli [40]. A lack of these identities cause controlled experiments to be difficult to execute, as capturing stimuli in the environment has proved difficult [27]. However, few stimuli have been identified as specific amino acids and other metabolic byproducts [51].
Climate change is progressing at an accelerated and unanticipated rate, significantly impacting marine organisms [47]. It is imperative to consider its role in assessing the effects of ocean acidification and warming of seawater on crustaceans [57]. Across the terrestrial and aquatic realms, crustaceans of either are facing environmental changes that drastically alter chemoreception [47]: the potency of chemical stimuli is declining, and consequently, the composition of stimuli [14]. This declination impairs conventional and appropriate behaviors, namely foraging efficiency, interactions with conspecifics, and predator detection [14].
Describing the benthic boundary layer (BBL)
Most Brachyurans are benthic organisms, which are defined as living on, in, or near the seabed [61]. They are adapted to withstand the strenuous conditions of the surrounding environment, specifically those characteristic of the benthic boundary layer (BBL)- the interface between the seafloor and the water column immediately above it [75]. Turbulence is characteristically high within these areas, where sediment is continuously falling and resuspending [73]. The BBL ranges in size from centimeters to meters in width, with eddies and vortices dominating the transport of matter [31]. Despite their irregular and nonuniform nature, these layers remain vertically stratified into two sublayers, which differ in transporting mechanisms [75].
The logarithmic layer is the uppermost layer and comprises most of the BBL (Lorke & MacIntrye 2009). This layer is designated as fully turbulent and experiences high levels of mixing. Vertical transport of stimuli is efficient and travels almost unpredictably [71]. It is influenced by the structure of the seafloor, also named bottom roughness, the source of momentum dissipation to form turbulence. The logarithmic layer is the environment brachyurans will utilize to locate distant sources of stimuli. As chemical plumes are formed and dispersed within the layer, they are immediately mixed and distributed by eddies- brachyurans obtain most olfactory information here [71]. The next layer is the viscous or diffusive sublayer, also known as the laminar sublayer (Lorke & MacIntyre 2009). Turbulent eddies are reduced by the friction adjacent to the seafloor, leaving the sublayer flowing smoothly. Vertical transport occurs slowly and is primarily governed by molecular diffusion- rather than turbulence [71]. It is the thinnest layer, fluctuating from micrometers to a few millimeters. Distributed chemoreception operates within this layer, particularly upon the dactyls. This slow rate of transport allows for the development of concentration gradients to reach high threshold sensory receptors (Angel & Boxshall 1990).
Turbulent hydrodynamics strongly influence the dispersion and attenuation of plumes and are therefore relevant to evaluate [61]. The flow fields and patterns within the BBL dictate the flow regime of the plume [75], which can be further evaluated by Reynolds’ number (Re) [31]. The Reynolds number is a ratio of inertial to viscous forces in flow regimes, which are the forces governing how turbulent plumes disperse within the water column and boundary layer [71]. High Reynolds numbers represent turbulent and chaotic flows, where chemical signals break into intermittent and unpredictable filaments [73]; eddies and vortices characterize these flows [30]. Whereas low Reynolds numbers represent laminar flows with fluid moving parallel with slight mixing [30].
Chemosensory ecology & behavior
Numerous defining characteristics add to the constant turbulence of the layer [73]. Sediment transport creates noise within the water column that complicates plumes traveling through [44]. Transportation of particles within the water column and BBL occurs in modes of bedload, washload, and suspension. In addition to these modes, the BBL is a hotspot for biological, geological, and chemical cycling (Lorke & MacIntrye 2009).
Seabed stress is high, so brachyurans display various strategies of locomotion, such as lateral walking and burrowing [22]. Post-larval crabs routinely settle within these areas, making these turbulent areas their settlements [73]. Distinctively, brachyurans are bioturbators- they disturb sediment [4]. Of these mentioned, all are examples of behaviors that routinely stir up sediment, which influences the immediate turbulence around the brachyuran (Lorke & MacIntrye 2009).
Chemoreceptive behaviors that Brachyurans characteristically exhibit include probing the substrate with their dactyls on the pereiopods [18]. Once the crab’s receptors capture a stimulus, they typically retreat in a defensive manner [49]. Terrestrial crabs, such as hermit crabs, retract into their shells [26]. Standardly, an increase in hiding time has been recorded across studies regarding this foraging behavior. Discrimination between predator effluents vs non-predatory effluents has also been recorded, as many brachyurans can identify conspecifics [5],[49]. Upon identification, assessment of a conspecific’s social status often occurs. Size or quality of shell are factors that features that may strike as dominant.
Brachyurans extract olfactory information from a variant flow field by rapidly flicking their antennae, a behavior analogous to a “sniff” [69]. The efficiency of flicking relies on the aesthetasc array in relation to its critical velocity range [54]. Capturing occurs within a rapid downstroke of the antennule, which generates a movement quicker than critical velocity [54],[61]. The aesthetic array leaves room for stimuli to flow in between the spaces of each aesthetasc, bringing chemical filaments closer to the receptors [69]. Trapping occurs when the antennule returns back to its original position; it moves slower than the critical velocity [54]: the aesthetic array traps the initial stimuli sampled during the flick (Koehl, 2011). Olfactory receptors acquire this information when the initial molecules diffuse from the water trapped between the aesthetascs, before the subsequent flick [69]. This process provides chemosensory information within 500-600 milliseconds [54].
Effective sampling requires a high Re downstroke and a low Re return stroke; this is a simpler process if the immediate environment has a lower Re value [54]. It is critical that the water containing the stimuli is trapped and penetrates the array; complex and turbulent environments disturb this process (Koehl, 2011) [69]. The Re value of flows in relation to foraging has been studied, with foraging efficiency decreasing as Re values increase [56]. Carcinus maenas, the green crab, demonstrates weaker foraging efficiency when experiencing high Re values [56]; the observed impairment was attributed to the immediate turbulent area, which hindered the brachyuran’s ability to locate prey [56]. Conversely, relatively laminar flows allowed plumes to remain coherent, thereby enhancing prey tracking and localization [49].
Flexibility of aesthetascs is a characteristic shown in many brachyuran species, such as the blue crab (Callinectes sapidus) and the shore crab (Hemigrapsus oregonesis) [69]. Flexibility allows aesthetascs to “splay” apart during the initial downstroke, therefore allowing a larger concentration of stimuli to flow between the aesthetasc gaps (Koehl, 2011). The aesthetascs clump together upon the slower return stroke to trap the stimuli more efficiently [69]. These dense and flexible aesthetascs are specialized for a hydrodynamic environment, allowing for the peripheral system to accurately and precisely acquire fine-scale spatio-temporal stimuli [44].
Contact chemoreception occurring on the dactyls assists in feeding, substrate exploration and interaction with conspecifics [60]. Analagous to gustation, dactyls require direct physical contact with the source to receive both chemoreceptive and mechanoreceptive information [43]. The sensilla located on the dactyls are cuticular with a thick, non-permeable wall, containing one terminal pore at the tip, where stimuli enter. Chemical stimuli diffuse through this pore and interact with dendrites [71]. Dactyls detect the presence of spilled or buried prey upon contact (Davie et al. 2015). It is hypothesized that dactyl chemoreception assists in habitat selection, given observations that brachyurans exhibit preferences for particular sediment types, water parameters, and the presence of certain macroalgae (Davie et al. 2015).
The maxillipeds, located on the mouth apparatus, aid in contact chemoreception [60]. Sensilla possess a terminal pore at the tip, where food is manipulated and placed in the mouth region [10]. This is where edible versus inedible material is distinguished [3]. The oesophagus plays a role in rejection of material if high concentrations of deterrents like toxins or secondary metabolites are present [17].
Ionotropic Receptors (IRs) and chemical stimuli discrimination.
Ionotropic receptors (IRs) serve as the primary olfactory receptors in brachyurans, playing a critical role in the detection and discrimination of stimuli within the BBL [17]. The evolutionary origin of these IRs- descended from ionotropic glutamate receptors (iGluRs), are known for mediating fast synaptic transmission within the CNS [11]. The capacity of brachyurans to quickly attain high-resolution olfactory information and rapidly respond is primarily dependent upon the Ionotropic Receptor (IR) family [19],[72].
Current transcriptomic data for Brachyura are highly concentrated around C. sapidus, leaving a significant knowledge gap in expression profiles for non-model species. However, C. sapidus transcriptomic analyses reveal hundreds of IRs, alongside additional chemoreceptor proteins [19]. IRs are localized on the dendritic membranes of the Olfactory Sensory Neurons (OSNs), within the aesthetascs [20]. IRs act as ligand-gated ion channels, thereby opening their channels when a particular odorant molecule (the ligand) binds to a receptor [28]. As the channel opens, cations rapidly pour into the sensory neuron, which depolarizes the cell and creates an electrical signal [19]. This signal is then transmitted to the OL [13]. Though IRs are expressed primarily within the olfactory pathway, some evidence suggests relatives of the IR family are present within the distributed chemosensory pathway [2],[20]. This area of research is less extensive, as much of brachyuran chemosensory research regards olfaction [1].
IRs are functionally divided into minimal co-receptor IRs and abundant tuning IRs [1]. The co-receptor IRs form the ion channel itself- the tuning IRs possess a role in ligand discrimination and chemical specificity. The copious numbers of IRs, specifically those expressed in the antennule’s lateral flagellum, reflect the highly specialized nature of brachyuran olfactory processing [40],[2010]. Though numerous, there are minimal types of IRs that must distinguish between a wide variety of chemical stimuli [17],[52]. Brachyuran inhabit a chemically complex environment, necessitating the discrimination of a vast array of compounds crucial for survival [2]. Considering the exceedingly small family of candidate olfactory receptors, there is a great challenge in understanding how one receptor per one ligand functions to create a vast specificity [9],[13]. Additionally, it is unknown where the CNS fits within this olfactory receptor coding paradox and the specificity of each IR complex [20].
Chemical stimuli are complex and consist of multiple elements; the capturing of these components has been stifled by methodological challenges [65]. Research has focused on two major classes of biologically relevant molecules: signals and cues [28]. Signals, or pheromones, play a crucial role in social interactions [9],[25]. In several brachyuran species, female ecdysis (molting) serves as a stimulus for initiating male courtship behaviors [25],[32],[50]. The second class consists of chemical cues, defined as byproducts of an organism or the environment [65]. Overall, potent and ubiquitous foraging cues are often water-soluble molecules that signal the breakdown or presence of organic matter [53]. This stimulus is detected inadvertently and is crucial for identifying potential predators and foraging [28]. Functionally, predator-related cues are classified as repellents or alarms, while foraging-related cues are termed attractants [53].
Compound identification and characterization is a significant research gap that grows further, as stimuli vary among species and prey [65]. Amino acids like L-Glutamate, L-Proline, and Glycine are strong attractants for crab species such as the Chinese mitten crab (Eriocheir sinensis) [50]. Betaines and quaternary ammonium compounds (QACs) are osmolytes that are effective at stimulating feeding behavior, contrasting with predatorial cues that retain traces of metabolites within urine, faeces, or mucus [11],[28]. Amine compounds and non-volatile steroids are commonly excreted from these byproducts, as well as injuries from a predator or conspecific [53](Potocka & Stainislaw, 2004); The haemolymph of brachyurans contains amino acids and peptides associated with crushed limbs that act as alarm signals [24].
Integration of Olfactory, Mechanosensory & Chemosensory Pathways
To combine all pathways, olfaction, mechanoreception, and chemoreception means to combine separate modes of chemical processing [41],[59]. The CNS of brachyurans has evolved to combine chemosensory and mechanosensory functions early upon chemical capture [43]: this enhances foraging behavior within the BBL and aids the crustaceans in navigating plumes of chemical significance [17],[59]. Various electrophysiological studies have shown that local interneurons (LNs), located within the deutocerebrum, obtain input from aesthetasc chemoreceptors (olfaction) as well as hydrodynamic flow detections (mechanoreception) [17]. Brachyurans rapidly analyze hydrodynamic flow regimes through this integration process: olfactory and mechanosensory [2]. This combined sensory input unifies the organism’s distributed chemosensory system with the olfactory [13]. The integration of mechanosensory input with olfactory input (odorants) leads to an amplification of information within the deutocerebral interneurons (Krieger et al. 2012). This form of integration acts as a filter, allowing frail chemical cues and signals to become amplified whenever they are captured within desired fluid [20].
Neurologically, mechanoreception occurs as near-field input from the MRNs projects to the Medial Antennular Neuropil (MAN) [20]. PNs within the MAN relay this information to the Protocerebrum (PCP) (Krieger et al. 2012). Conversely, olfaction pathways occur as the CRNs project directly into the Deutocerebrum, where the OL is located [39],[59]. After reaching the OL, PNs relay the processed signal to the PCP as well. Integration continues and moves towards the Medulla Terminalis (MT) [62]. The Medulla Terminalis (MT) is associated with vision, motor control, and limb coordination [20]. This high-level integration center lies within the protocerebrum and acts as the largest neuropil within the eyestock [39]. It is the receiving center from the LAN and OL (Krieger et al. 2012). Distributed chemosensory itself is associated with the PCP, but bypasses the OL and MAN; it is speculated that the pathway interacts with the MT, but it is not associated with it [59]. Though convergence occurs within the PCP, the actual integration process results in a behavioral response [20].
Impacts of climate change on brachyuran chemoreception
Climate change exerts a profound impact on the production, transmission, and reception of chemical and physical stimuli [14]. Ocean acidification is the primary driver of sensory disruption, stemming from an increased absorption of atmospheric carbon dioxide [47]. The decrease in ocean pH facilitates an increase of hydrogen ions present, altering the structural integrity of stimuli [57]. Consequently, compounds such as amino acids are impacted as they are released, and inhibit proper binding to chemoreceptor proteins on the aesthetascs [52]. A failure of this binding will suppress the ability to engage in essential behaviors, such as defensive, foraging, and recognition behaviors [47].
Overall, the function of the crustacean nervous system is dependent upon precise acid-base regulation [3], which is compromised by environmental pH changes. This disruption interferes with essential neuronal processes, including maintenance of ion gradients and formation of neurotransmitter systems in the central and peripheral nervous systems [14]. The result could trigger failed attempts of signal transduction that will ultimately result in a faulty neural processing system and dysfunctional behavior [14]. An increase in late pheromone detection by male brachyurans is exhibited, as well as an overall decrease in sexual activity. Though detection occurs earlier, mating behavior is reduced [47]. Behavioral anomalies such are attributed to altered pheromone structure and impaired receptor function, as mentioned above [14].
Elevated water temperatures influence chemoreception on ecologically as well as biologically [17]. Higher temperatures drive higher metabolic rates in brachyurans, increasing oxygen demand and stress [57]. This physiological stress necessitates a greater allocation of energy towards current survival strategies, diverting resources away from complex sensory processes [14]. Hydrodynamic changes could occur within the BBL, which directly controls chemical transport (Sweetman et al. 2017). Predicated hydrodynamic alterations include an increase in storm turbulence, reduced mixing and therefore greater stratification, and an overall change to the current benthos (Leeder et al. 1998).
Increased terrestrial temperatures can drive increasingly intense storms and cyclones, generating stronger wind-driven currents and waves (Vanem et al. 2012). Heightened forces will influence bed shear stress- the frictional force per unit area exerted by fluid against a substrate (Leeder et al. 1998). This process lifts bottom sediments, which creates turbulent plumes in the process; frequent and more intense sediment resuspension will occur as a result (Sweetman et al. 2017). Higher stresses will lead to higher turbulence, leaving organisms to find strong attachment mechanisms to survive [75]. This alteration could impact light penetration, affecting primary productivity within the environment. Furthermore, warming waters display a pattern of strong thermal stratification, which can strongly suppress vertical mixing (Sweetman et al. 2017). Isolating the BBL could occur, as water flow would become more laminar. Oxygen within the layers would become isolated, and hypoxia could occur.
Combining techniques in hydrodynamics and neurophysiology
Despite significant advances in the identification and relationship of neuroanatomical pathways and chemical signaling, a comprehensive understanding of the central algorithms that drive behavior is needed [20]. Consequently, neurophysiological investigations have relied on controlled and static conditions, failing to replicate the complex and turbulent plumes that brachyurans analyze for survival [29]. Analysis of benthic neuroethology reveals that there are significant knowledge gaps that constrain further research: the insufficient identification of chemical compounds that mediate behavior and a poor understanding of the CNS pathways responsible for integrating and utilizing chemical signals.
A bottleneck is occurring at this point, where researchers are unable to link behaviors to specific IRs and their individual coding patterns. A chemical deficit prevents researchers from establishing a link between molecular and behavioral levels of analysis [27]. There is a lack of confirmed identity among specific ligands and mixtures that mediate behavior. Confidently mapping cues and signals to profiles of relevant IRs to decode their coding patterns cannot be completed without doing so. Molecular and physiological data have given way to how the peripheral system can capture high-resolution input, but little knowledge to how the CNS interprets that complex code [20]. A mechanistic understanding of how receptors contribute to the code represents a great research investment. The future of resolving difficult topics, such as the olfactory coding paradox, necessitates adopting interdisciplinary approaches that have limited groundwork to date.
In resolving central utilization gaps, experimental techniques in fluid physics are needed for the marine benthic realm [27]: coupling quantitative fluid physics and neurophysiology could prove to close these gaps in the future. The question of CNS decoding odor plumes necessitates more than static olfactometers and instead requires more suitable equipment to measure highly turbulent, filamentous plumes found in the BBL [20]. Utilizing Planar Laser-Induced Fluorescence (PLIF) is one technique that could aid in visualizing and quantifying concentrations within a flow regime [73]. Stimulus control would have to be paired with a quantitative central neural technique, such as calcium imaging or voltage-sensitive dye imaging [37],[46]. Application would occur within the brachyuran OL and MT, which would allow researchers to observe in real time the activity of PNs and local interneurons interacting with an odor plume [13]. This could allow researchers to put together a temporal structure of the cue or signal, with the neural firing patterns that follow stimulation. From here, the ability to interpret peripheral temporal code could become available and aid in navigating various benthic brachyuran neurophysiology.
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Cover Image: https://www.underwaterkwaj.com/uw-misc/crab/Calappa-calappa.htm
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