All nervous systems are multiply modulated by polypeptides. However, a bulk of transmitter and modulation research has historically focused on small molecule transmitters released at synaptic sites. The stomatogastric nervous system (controls digestive movements of the foregut) and cardiac nervous system of decapod crustaceans have long been used to understand the processes that underlie neuromodulation. The circuits governing the rhythmic output from these nervous systems are comprised of a relatively small number of identified neurons, and the details of these nervous systems are well-defined. Here we discuss recent research highlighting advances in our understanding of peptidergic modulation in these systems. In particular, we focus on our ability to identify specific signaling peptide sequences and relate their expression patterns to their physiological effects, as well as on the multiple sites within a pattern generator-effector system at which modulation takes place. Recent efforts have enabled us to understand how co-modulation by two or more peptides can generate surprising effects on circuit physiology and that modulation at different receptor sites can produce supra-additive effects. Finally, we examine the protective role modulation plays in making circuits robust to perturbations, in this case, changes in temperature. 

Diversity of neuropeptidergic modulation in decapod crustacean cardiac and feeding systems

ABSTRACT Until recently, the decapod crustacean heart was regarded as a simple, single ventricle, contraction of which forces haemolymph out into seven arteries. Differential tissue perfusion is achieved by contraction and relaxation of valves at the base of each artery. In this Review, we discuss recent work that has shown that the heart is bifurcated by muscular sheets that may effectively divide the single ventricle into ‘chambers’. Preliminary research shows that these chambers may contract differentially; whether this enables selective tissue perfusion remains to be seen. Crustaceans are unusual in that they can stop their heart for extended periods. These periods of cardiac arrest can become remarkably rhythmic, accounting for a significant portion of the cardiac repertoire. As we discuss in this Review, in crustaceans, changes in heart rate have been used extensively as a measurement of stress and metabolism. We suggest that the periods of cardiac pausing should also be quantified in this context. In the past three decades, an exponential increase in crustacean aquaculture has occurred and heart rate (and changes thereof) is being used to understand the stress responses of farmed crustaceans, as well as providing an indicator of disease progression. Furthermore, as summarized in this Review, heart rate is now being used as an effective indicator of humane methods to anaesthetize, stun or euthanize crustaceans destined for the table or for use in scientific research. We believe that incorporation of new biomedical technology and new animal welfare policies will guide future research directions in this field. 

Cardiovascular physiology of decapod crustaceans: from scientific inquiry to practical applications

Behavioral thermoregulation of ovigerous American lobsters (Homarus americanus)

Animals of all kinds evolved to deal with anticipated and unanticipated changes in a variety of features in their environments. Consequently, all environmental perturbations, adaptations, and acclimation involve a myriad of factors that, together, contribute to environmental resilience. New work highlights the importance of neuromodulation in the control of environmental resilience, and illustrates that different components of the nervous system may be differentially resilient to environmental perturbations. Climate change is today pushing animals to deal with previously unanticipated environmental challenges, and therefore understanding the complex biology of adaptation and acclimation to various environmental conditions takes on new urgency. 

Resilience of circuits to environmental challenge

Decapod crustaceans provide a valuable food source worldwide, both through wild capture and captive rearing. They are also used extensively in scientific research, both as subjects for the investigation of basic biological processes and as model organisms for the detection of environmental changes. There is now an increasing acceptance that decapod crustaceans are sentient, and legislation is being introduced in numerous countries to ensure crustacean welfare when they are harvested or held captive. Moreover, methods for the humane slaughter of these animals are being developed, and of these electrical stunning is a prime candidate. Optimisation of electrical stunning is underway for a range of commercially-exploited or scientifically-important species, and the present study contributes to that process by examining further crab (Carcinus maenas) and lobster (Homarus gammarus) species using a rigorous neurophysiological approach. By recording nerve activity in both the central and peripheral nervous systems, we have found that electrical stunning with a standard commercial instrument arrests nerve activity in both these species at all levels: sensory, motor and central, rendering the animals neurologically insensible. This methodology is the most direct and effective way to establish if insensibility is successfully achieved. However, ultimately the routine monitoring of effective stunning in commercial and laboratory settings will have to depend on simple, yet reliable physiological or behavioural indicators, following their calibration against neurological methods. Monitoring heartbeat is used widely to establish metabolic activity, locomotory performance, agonistic interactions and responses to environmental conditions. We have therefore assessed the potential to use cardiac activity as an indicator for the state of sensibility. We recorded the heartbeat in both C. maenas and H. gammarus before and after electrical stunning, but find that in many cases even though nerve activity has ceased both centrally and peripherally, cardiac activity actually continues (though at a reduced rate) for a substantial time (>1h). The heartbeat is therefore not a reliable indicator of the state of sensibility, making it an unsuitable indicator of effective stunning. Possible reasons for these findings, and ways to validate behavioural measures that may be more appropriate for routinely establishing effective electrical stunning, are discussed.

Towards the humane slaughter of decapod crustaceans: identifying the most effective indicators of insensibility following electrical stunning

Changes in ambient temperature affect all biological processes. However, these effects are process specific and often vary non-linearly. It is thus a non-trivial problem for neuronal circuits to maintain coordinated, functional output across a range of temperatures. The cardiac nervous systems in two species of decapod crustaceans, Homarus americanus and Cancer borealis, can maintain function across a wide but physiologically relevant temperature range. However, the processes that underlie temperature resilience in neuronal circuits and muscle systems are not fully understood. Here, we demonstrate that the non-isolated cardiac nervous system (i.e., the whole heart: neurons, effector organs, intrinsic feedback systems) in the American lobster, H. americanus, is more sensitive to warm temperatures than the isolated cardiac ganglion (CG) that controls the heartbeat. This was surprising as modulatory processes known to stabilize the output from the CG are absent when the ganglion is isolated. One source of inhibitory feedback in the intact cardiac neuromuscular system is nitric oxide (NO), which is released in response to heart contractions. We hypothesized that the greater temperature tolerance observed in the isolated CG is due to the absence of NO feedback. Here, we demonstrate that applying an NO donor to the isolated CG reduces its temperature tolerance. Similarly, we show that the NO synthase inhibitor L-nitroarginine (LNA) increases the temperature tolerance of the non-isolated nervous system. This is sufficient to explain differences in temperature tolerance between the isolated CG and the whole heart. However, in an intact lobster, the heart and CG are modulated by an array of endogenous peptides and hormones, many of which are positive regulators of the heartbeat. Many studies have demonstrated that excitatory modulators increase temperature resilience. However, this neuromuscular system is regulated by both excitatory and inhibitory peptide modulators. Perfusing SGRNFLRFamide, a FLRFamide-like peptide, through the heart increases the non-isolated nervous system’s tolerance to high temperatures. In contrast, perfusing myosuppressin, a peptide that negatively regulates the heartbeat frequency, decreases the temperature tolerance. Our data suggest that, in this nervous system, positive regulators of neural output increase temperature tolerance of the neuromuscular system, while modulators that decrease neural output decrease temperature tolerance.

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The role of feedback and modulation in determining temperature resiliency in the lobster cardiac nervous system

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The role of feedback and modulation in determining temperature resiliency in the lobster cardiac nervous system