Low metabolic rate in scorpions: implications for population biomass and cannibalism.

Scorpions are abundant in arid areas, where their population biomass may exceed that of vertebrates. Since scorpions are predators of small arthropods and feed infrequently across multi-year lifespans, a parsimonious explanation for their observed, anomalously high biomass may be a depressed metabolic rate (MR). We tested the hypothesis that scorpion MR is significantly depressed compared with that of other arthropods, and we also measured the temperature-dependence of the MR of scorpions to quantify the interaction between large seasonal variations in desert temperatures and MR and, thus, long-term metabolic expenditure. Scorpion MR increased markedly with temperature (mean Q(10)=2.97) with considerable inter-individual variation. At 25 degrees C, the MRs of scorpions from two genera were less than 24 % of those of typical terrestrial arthropods (spiders, mites, solpugids and insects) of the same mass. It is likely, therefore, that the low MR of scorpions contributes to their high biomass in arid areas. The combination of high biomass and high production efficiency associated with low MR may also favor a density-dependent "transgenerational energy storage" strategy, whereby juveniles are harvested by cannibalistic adults that may be closely related to their juvenile prey.

Glomerular cytoarchitectures in chemosensory systems of arachnids.

In most animals the central pathways of olfactory systems are associated with glomerular neuropil and lack topographic mapping of sensory inputs. Among arthropods, the insect and crustacean olfactory (antennal) pathways are typical examples. Two orders of chelicerate arthropods, the scorpions and solpugids (Cl. Arachnida), present striking exceptions to this generalization. The major chemosensory organs of scorpions are the pectines, two ventral appendages that contact the substrate intermittently as the animal searches for food or mates. In solpugids chemosensory input is from the antennalized pedipalps and first leg pairs, and from ten fan-shaped malleoli extending ventrally to the substrate from the 4th leg pair. The pectinal and malleolar sensory systems have highly ordered arrangement of 10(5) to 10(6) primary chemoreceptors, with one (pectines) forming a two-dimensional array and the other (malleoli) assembled in a linear array. The spatial frequencies of these chemoreceptive inputs exceed 100/mm and 1000/mm, respectively, indicating a capacity for resolving structure of chemical deposits on substrates. Using several histological and axonal tracing techniques, the organization of pectinal and malleolar central projections has been resolved. The pectinal projection terminates posteriorly in the cephalothoracic mass and shows a high degree of topographic precision, perhaps to the level of individual receptors in the sensory field. This chemosensory 'map' is imposed on laminar cytoarchitecture posteriorly in the brain but merges anteriorly into glomerular substructures. The sensory projection from the malleoli shows less topographic order with fewer and larger glomeruli reminiscent of the insect olfactory system. These comparisons between arthropod taxa suggest that olfactory projections are, to varying degrees, typically glomerular but may evolve topographic and laminar organization when the stimulus field is of fixed form.

Response properties of chemosensory peg sensilla on the pectines of scorpions.

By behavioral and anatomical criteria, the pectinal sensory appendages of scorpions appear to be chemoreceptive organs specialized for detection of substances on substrates. These comb-like, midventral appendages contain tens of thousands of minute (< 5 microns), truncated setae, called pegs, arranged in dense, two-dimensional arrays on the ventral surface. In this study we used extracellular recording techniques to examine spontaneous and stimulated activity of sensory neurons within individual pegs. Chronic recordings lasting several days showed long-term fluctuations in spontaneous activity of sensory units in single peg sensilla, with peak activity coinciding with the animal's normal period of foraging. Several units were identified by the stereotypical waveforms of action potentials they elicit. Near-range olfactory stimulation of peg sensilla by volatile alcohols, aldehydes, ketones, esters, and carboxylic acids produced dose-dependent patterns of neural response. Contact stimulation with these chemicals, or water, or mechanical deflection of the peg tip also evoked activity in identifiable units. The peg sensilla appear to be broadly sensitive to odorants and tastants, suggesting they function similarly to the antennae of mandibulate arthropods.

Electrophysiological evidence of synaptic interactions within chemosensory sensilla of scorpion pectines.

The pectines of scorpions are ventral bilateral appendages supporting 10(4)-10(5) chemosensory sensilla called pegs. Each peg contains 10-18 sensory neurons, some of which show ultrastructural evidence of axo-axonic synapses with other sensory neurons in the same sensillum. In extracellular recordings from single-peg sensilla, individual sensory units can be distinguished by impulse waveform and firing frequency. Cross-correlation analysis of impulse activity showed that at least two of these units, types 'A1' and 'A2', are inhibited during the 100-ms period immediately following activity of a third unit, type 'B'. This interaction between sensory units in a single sensillum also occurs in surgically isolated pectines, indicating that it does not involve efferent feedback from the central nervous system. Other sensillar neurons appear to have excitatory interactions. Thus, in scorpion pectine, chemosensory information undergoes some form of processing within individual sensilla prior to its relay to the CNS, making this an unusually accessible preparation for study of first-order chemosensory processing events.

Neurotransmitter regulation of the heart in the nudibranch Archidoris montereyensis.

1. The heart of the nudibranch mollusc Archidoris montereyensis is uniquely responsive to regulation by identifiable cardiac motor neurons. The neurotransmitters mediating the strong excitatory and inhibitory actions of the neurons are unknown. 2. In this study we developed an infused, in vitro preparation of the Archidoris heart to determine which of several cardioactive transmitters described in mollusks could affect changes in the rate, amplitude, or tonus of cardiac contractions. Several neurotransmitters we tested increased the rate and amplitude of heart contractions, including serotonin (threshold < 10 nM), dopamine (100 nM), and the neuropeptides R15 alpha 2 (3 nM), small cardioactive peptide B (10 nM), and FMRFamide (20 microM). Myomodulin also excited the heart (0.8 microM) and potentiated the cardioexcitatory action of serotonin at subthreshold concentrations. 3. Only acetylcholine (10 nM) inhibited the heart, decreasing the rate, amplitude, and tonus of contraction. Glycine and the peptides substance P and R15 alpha 1 had no effect on the heart. 4. Antisera against the active neurotransmitters labeled central neurons and nerves innervating the heart in a pattern consistent with their putative cardioregulatory functions. 5. Thus, despite the simplicity of the cardiac motor circuit in Archidoris, contractile activity of the heart appears to be regulated by several neurotransmitters, each with subtly different modes and thresholds of action.

Neuroendocrine control of egg-laying behavior in the nudibranch, Archidoris montereyensis.

We describe a group of neurons with egg-laying bioactivity in the cerebral ganglia of an opisthobranch mollusc, the nudibranch Archidoris montereyensis. These cells, the intercerebral white cells (IWCs), share morphological, biochemical, and electrophysiological characteristics with the egg-laying neuroendocrine cells of two other molluscs, Aplysia californica (bag cells) and Lymnaea stagnalis (caudodorsal cells). The IWCs, comprising two superficial clusters of about 100 neurons each, were located immediately posterior to the intercerebral commissure in the cerebral ganglia. The somata of these cells were small (< 20 microns) and possessed varicose, bifurcating unipolar processes that collectively formed a loop within the commissure and bilateral extensions into the cerebral ganglia. The IWC clusters and commissural processes were enveloped by a large ganglionic vascular sinus, forming a potential neurohemal release site. Homogenates of whole cerebral ganglia or isolated IWC clusters induced egg-laying behavior within hours of injection into the hemocoel of quiescent animals. The IWCs were immunoreactive for alpha bag-cell peptide, one of the neuropeptide transmitters encoded by the egg-laying hormone gene of Aplysia. Electrophysiologically, the IWCs were silent neurons with large resting potentials and appeared to be highly refractory to electrical stimulation. The similarities of the IWCs to the egg-laying neuroendocrine cells in Aplysia and Lymnaea suggest that they are members of a homologous group of neurons controlling egg-laying behavior in gastropod molluscs.

Mechanisms of circulatory homeostasis and response in Aplysia.

This review concerns the organization and function of arterial vasculature in Aplysia californica, especially the vasomotor reflexes that support circulatory homeostasis, and fixed patterns of response that may reroute blood flow during changes in behavioral state. The observations presented here raise three hypotheses for further study: 1) Arterial vasculature is functionally organized with precisely structured, independently regulated subdivisions; these are most evident for arterial systems serving digestive and reproductive processes; 2) arterial musculature is inherently responsive to local pressure changes, having both static and dynamic reflexes that promote efficient, evenly-distributed flow of blood; and 3) complex, long-lasting behaviors like egg laying have, as part of their makeup, equally prolonged and stereotypical changes in the pattern of circulation. Taken together, these observations support the view that maintenance and adjustment of blood flow in gastropod molluscs is an unexpectedly complex and highly integrated component of behavior.

Characterization of cardiac innervation in the nudibranch, Archidoris montereyensis.

The heart of the nudibranch mollusc Archidoris montereyensis is regulated by a small number of powerful effector neurons located in the right pleural and visceral ganglia. Two identifiable neurons in the pleural ganglion, a heart excitor (PlHE) and a heart inhibitor (PlHI), are especially important regulators of cardiac function in that low levels of spontaneous activity in either cell significantly alters the amplitude and rate of heart contractions. These neurons have extensive dendritic arbors within the right pleural ganglion and branching axonal processes within the visceral ganglion. The visceral ganglion also contains a heart excitor neuron (VHE) and at least two heart inhibitor neurons (VHI cells), but their influence on cardiac activity is weaker than that of the pleural ganglion cells. All of these heart effector cells appear to be motor neurons with axons that terminate predominantly in the atrio-ventricular valve region of the heart via the pericardial nerve. The simplicity and strength of these neuronal connections to the heart of Archidoris make this a favorable preparation for studies of cardiac regulation.

Ganglionic circulation and its effects on neurons controlling cardiovascular functions in Aplysia californica.

The abdominal ganglion of the mollusk Aplysia californica receives most of its blood supply through a small caudal artery that branches off the anterior aorta near its junction with the heart. Injection of an ink/gelatin mixture into the caudal artery revealed a consistent pattern of arterial branching within the ganglion and a general proximity of larger vessels to identified neurons controlling circulation in this animal. This morphological arrangement was particularly evident for the heart excitor interneuron, cell L10, which lies next to the caudal artery near its entry into the ganglion. In electrophysiological experiments, L10 was excited when blood flow or oxygen tension within the ganglion was reduced. This effect was expressed as a gradual increase in impulse frequency of L10 and conversion from tonic to bursting mode of spike discharge. L10 follower cells in the RB and LD neuron clusters were affected synaptically by the changes in L10 activity, while other follower cells (L3 and RD neurons) responded independently of L10's synaptic influence. The neurosecretory white cells (R3 to R14) that innervate the major arteries and pericardial tissues were also excited when ganglionic circulation was interrupted. In innervated preparations of the heart and respiratory organs, decreased circulation through the abdominal ganglion stimulated a transient increase in the rate and amplitude of respiratory (gill) pumping and pericardial contractions and caused a sustained increase in activity of the heart. Both responses increase cardiac output and both appear to involve a direct influence of ganglionic circulation on interneurons controlling the gill and heart. These results indicate that the cell-specific patterns of excitation and inhibition caused by fluctuations in ganglionic circulation may be important factors for maintaining circulatory homeostasis in this animal.

Modulation of a respiratory motor program by peptide-secreting neurons in Aplysia.

Respiratory pumping of the gill and siphon of Aplysia californica is a fixed-action pattern coordinated by a defined set of interneurons and motor neurons. In semi-intact preparations of the gill and siphon innervated by the abdominal ganglion, respiratory pumping is facilitated for a prolonged period following activation of the peptidergic bag cell neurons. The induced changes in contractile behavior of the gill and siphon correlate with cell-specific actions of the bag cells on motor neurons regulating these organs. Our results suggest that peptidergic neurons can alter the expression of a fixed pattern of behavior by modulating the excitability of motor neurons controlling the behavior.

Activity-related changes in protein phosphorylation in an identified Aplysia neuron.

The relationship between long-term electrical activity and protein phosphorylation was investigated in single, identifiable neurons in the abdominal ganglion of Aplysia californica by the intracellular injection of radiolabeled ATP followed by sodium dodecyl sulfate (SDS) gel electrophoresis. Natural and pharmacological treatments that alter the impulse activity of neurons L6 and R15 for prolonged periods did not appear to affect the phosphorylation of most of the 15 major phosphoproteins examined in these cells. Long-term excitation of L6 induced by the phosphodiesterase inhibitor IBMX correlated with phosphorylation of a 29,000-dalton protein. Long-term inhibition of L6 induced by afterdischarge of peptidergic bag-cell neurons appeared to cause dephosphorylation of a 29,000-dalton protein. Burst augmentation of R15 induced by bag-cell afterdischarge did not cause detectable changes in the phosphorylation of the major proteins we examined. These data are consistent with other studies of neural and nonneural tissues which have found a correlation between activity and the level of phosphorylation of a 29,000-dalton protein.

Nonsynaptic characteristics of neurotransmission mediated by egg-laying hormone in the abdominal ganglion of Aplysia.

The bag cell neurons of the marine mollusk Aplysia are a putative multitransmitter system which utilizes two or more neuropeptides that are enzymatically cleaved from a common precursor protein. It has been proposed that one of the neuropeptides, egg-laying hormone (ELH), acts nonsynaptically as a neurotransmitter in the abdominal ganglion by diffusing long distances to target neurons compared to conventional transmitters acting at synapses. To test this idea further, we investigated the physiological properties of neurotransmission mediated by ELH. We found that ELH acts directly to duplicate two types of responses produced by a burst discharge of the bag cells: prolonged excitation of LB and LC cells, and the previously described effect of ELH, burst augmentation of cell R15. Analysis of perfusate collected after electrical stimulation of the bag cells showed that the peptide is released in sufficient quantity to diffuse long distances within the ganglion without being completely inactivated. To mimic the way the peptide is thought to be released physiologically, ELH was arterially perfused into the ganglion. The response normally produced by bag cell activity was duplicated by 0.5 to 1.0 microM concentrations of ELH and showed no rapid desensitization. ELH had no effect on cells that are unaffected by bag cell activity and no effect on cells that are inhibited (LUQ cells) or transiently excited (cells L1 and R1) by bag cell activity. Acidic peptide, another peptide encoded on the ELH precursor protein, was found to be synthesized and released by the bag cells, but it had no effect on the cells we tested. We conclude that the combined properties of ELH neurotransmission resemble the properties of transmission at autonomic nerve endings on cardiac and smooth muscle rather than those of conventional synaptic transmission. ELH released from bag cells is dispersed throughout the interstitial and vascular spaces of the ganglion to produce responses in the cells that have receptors for the peptide. The results also suggest that ELH mediates only a subset of the responses induced by bag cell activity; they are consistent with data indicating that the other responses are mediated by other bag cell peptides derived from the same precursor protein as ELH.

Differential hormonal action of the bag cell neurons on the arterial system of Aplysia.

The peptide-secreting bag cell neurons of Aplysia californica activate a long-lasting, complex behavior called egg laying. During egg laying some organ systems (reproductive) are more active than others (digestive) suggesting that blood flow to these tissues may change in accordance with their activities during egg laying. To examine this possibility we used a semi-intact preparation of the three major arteries innervated by the abdominal ganglion. We found that electrically stimulated bursts of bag cell activity triggered a long-lasting (greater than 1 h) increase in contractile activity in two arteries, the anterior and gastroesophageal, but did not affect contractions of the third (abdominal) artery. The arterial responses were not affected either in form or duration by denervation of the arteries, suggesting that the increase in contractile activity was mediated by hormonal actions of bag cell transmitters on vasoconstrictor muscles. In intact animals this differential action on the arterial system may cause a long-term decrease in blood flow to relatively inactive tissues (digestive and locomotory organs) while increasing circulation to tissues involved in egg production (ovotestis and oviduct).

Compressional and surface waves in sand: used by desert scorpions to locate prey.

Loose sand conducts compressional and surface (Rayleigh) waves at relatively low velocities (95 to 120 meters per second and 40 to 50 meters per second, respectively) compared to other natural substrates. For frequencies between 1 and 5 kilohertz, the specific attenuation factor, Q, for sand is 18. Compound slit sensilla on basitarsal leg segments of sand-dwelling scorpions respond to surface waves generated by movements of insects as far as 50 centimeters away, and tarsal sensory hairs respond to higher-frequency (mostly compressional-wave) components of the signal.