The cocoon of the developing emerald jewel wasp (Ampulex compressa) resists cannibalistic predation of the zombified host.

INTRODUCTION: To reproduce, the parasitoid emerald jewel wasp (Ampulex compressa) envenomates an American cockroach (Periplaneta americana) and barricades it in a hole with an egg on the host's leg. The larval wasp feeds externally before entering the host and consuming internal organs before forming a cocoon inside the host carcass. METHODS: The vulnerability of jewel wasp larvae to predation by juvenile cockroaches was investigated and data were recorded with time lapse videography. RESULTS: Cockroaches were found to be predators of parasitized hosts. When parasitized cockroaches were exposed to hungry cockroaches on days 0-8 of development, the developing larva was killed. Eggs were dislodged or consumed, larvae on the leg were eaten, and larva inside the host were eaten along with the host. On day 9, 80% of the wasp larvae were killed and eaten along with the host. Conversely, on day 10, 90% of the larvae survived. On developmental day 11 or later, the wasp larva always survived although the host carcass was consumed. Survival depended entirely on whether the cocoon had been completed. CONCLUSION: The results highlight the vulnerability of larvae to predation and suggest the cocoon defends from insect mandibles. This may explain the unusual feeding behavior of the jewel wasp larvae, which eat the host with remarkable speed, tapping into the host respiratory system in the process, and consumes vital organs early in contrast to many other parasitoids. Results are discussed in relation to larval wasp behavior, evolution, and development, and potential predators are considered.

Early destruction of cockroach respiratory system and heart by emerald jewel wasp larvae.

In the 1880s, Henri Fabre was captivated by the "special art of eating", whereby a parasitoid wasp larva fed selectively on host internal organs, avoiding the heart (dorsal vessel) and tracheal system (respiratory system) to preserve life. In Fabre's words: "The ruling feature in this scientific method of eating, which proceeds from parts less to the parts more necessary to preserve a remnant of life, is none the less obvious"1. Subsequent investigators have reported the same for many parasitoid wasps2,3, including for the emerald jewel wasp (Ampulex compressa)4. Here it is reported that larval jewel wasps destroy the dorsal vessel and tracheae (respiratory system) in the thorax of their cockroach host (Periplaneta americana) at their earliest opportunity. Moreover, the broken tracheae release air into the host, which the larval jewel wasp inspires. An increase in larval chewing rate, cotemporaneous with the sudden release of air from the host's broken tracheae, suggests the larva taps into the host respiratory system to support its metabolism while rapidly consuming the host. VIDEO ABSTRACT.

Tentacled snakes.

Catania provides an introduction to tentacled snakes and their ingenious ability to capture fish.

Electric Eels Wield a Functional Venom Analogue.

In this paper, I draw an analogy between the use of electricity by electric eels (Electrophorus electricus) to paralyze prey muscles and the use of venoms that paralyze prey by disrupting the neuromuscular junction. The eel's strategy depends on the recently discovered ability of eels to activate prey motor neuron efferents with high-voltage pulses. Usually, eels use high voltage to cause brief, whole-body tetanus, thus preventing escape while swallowing prey whole. However, when eels struggle with large prey, or with prey held precariously, they often curl to bring their tail to the opposite side. This more than doubles the strength of the electric field within shocked prey, ensuring maximal stimulation of motor neuron efferents. Eels then deliver repeated volleys of high-voltage pulses at a rate of approximately 100 Hz. This causes muscle fatigue that attenuates prey movement, thus preventing both escape and defense while the eel manipulates and swallows the helpless animal. Presumably, the evolution of enough electrical power to remotely activate ion channels in prey efferents sets the stage for the selection of eel behaviors that functionally "poison" prey muscles.

Getting the Most Out of Your Zombie: Abdominal Sensors and Neural Manipulations Help Jewel Wasps Find the Roach's Weak Spot.

The parasitoid emerald jewel wasp (Ampulex compressa) subdues the American cockroach (Periplaneta americana) with a sting to the 1st thoracic ganglion, followed by a sting to the roach's brain, causing long-term pacification. The wasp then leads the cockroach to a hole where it lays an egg on the roach middle leg before barricading the entrance and departing. Although many aspects of the wasp's initial attack have been investigated, few studies have detailed the egg-laying process and the subsequent fate of the larvae. Here I show that larval survival depends on precise egg positioning on the cockroach by the female wasp. Ablation of sensory hairs on the wasp's abdomen resulted in mislaid eggs, which seldom survived. In addition, the cockroach femur may block the oviposition site. The wasp contended with this challenge with a newly discovered suite of stings, 3 directed into the 2nd thoracic ganglion which resulted in extension of the femur, thus exposing the oviposition site and removing a potential barrier to the wasp's successful reproduction. When the femur was glued in place, the wasp stung the cockroach over 100 times, in an apparent fixed action pattern triggered by the obscured oviposition target. These findings highlight the importance of proper egg placement by the wasp, and reveal sensors and new neural manipulations that facilitate the process.

All in the Family - Touch Versus Olfaction in Moles.

Here I review, compare, and contrast the neurobiology and behavior of the common, eastern mole (Scalopus aquaticus) and the star-nosed mole (Condylura cristata). These two species are part of the same family (Talpidae) and have similar body size and general morphology. But they differ in sensory specializations, complexity of neocortical organization, and behavior. The star-nosed mole has an elaborate mechanosensory organ-the star-consisting of 22 epidermal appendages (rays) covered with 25,000 touch domes called Eimer's organs. This densely innervated structure is represented in the neocortex in three different somatosensory maps, each visible in flattened neocortical sections as a series of 11 modules representing the 11 rays from the contralateral body. The 11th ray is greatly magnified in primary somatosensory cortex (S1). Behavioral studies show the star is moved in a saccadic manner and the 11th ray is a high-resolution tactile fovea, allowing star-nosed moles to forage on small prey with unprecedented speed and efficiency. In contrast, common mole noses lack Eimer's organs, their neocortex contains only two cortical maps of the nose, and they cannot localize small prey. Yet common moles have exceptional olfactory abilities, sniffing in stereo to rapidly localize discrete odor sources originating from larger prey. In addition, common moles are shown to track odorant trails laid down by moving prey. These results highlight the surprising abilities of species once thought to be simple, and the usefulness of diverse species in revealing general principles of brain organization and behavior. Anat Rec, 2019. © 2019 American Association for Anatomy.

Unique features of the skin barrier in naked mole rats reflect adaptations to their fossorial habitat.

The stratum corneum (SC), the top layer of the epidermis, is the functional site of the skin barrier and serves to maintain hydration of the body by preventing water loss and thwarting the entrance of pathogens. The naked mole rat (NMR) (Heterocephalus glaber) is a rodent that resides in hypoxic underground tunnels in arid Africa. NMRs are not only hairless; their skin is devoid of glands and pain sensation. To understand how the skin barrier of the NMR is uniquely adapted to this environment, skin samples from the dorsum and ventral abdomen in one adult and one neonate were examined by transmission electron microscopy using both reduced osmium tetroxide to assess overall structure and ruthenium tetroxide post-fixation to assess lipid organization. These findings were compared with that of hairless mice-a well-defined model for skin barrier studies. The plasticity of the skin was evaluated on 10 NMRs from a colony at the Philadelphia Zoo in humid and dry conditions by measuring cutaneous hydration, transepidermal water loss (TEWL), and pH. The epidermal ultrastructure of the NMR differed from hairless mice by having the following features: decreased content of lamellar bodies (LBs), higher LB pleomorphism, periodic presence of abnormal lipid bilayers, and an unusually thick SC. The NMRs developed significant TEWL and a trend toward decreased hydration when subjected to dry conditions. While these features illustrate an imperfect skin barrier in terrestrial mammals, they likely represent adaptations of the poikilothermic NMRs to their unique natural fossorial climate. Prolonged exposure to decreased humidity could possibly lead to adverse health effects in this species.

The Astonishing Behavior of Electric Eels.

The remarkable physiology of the electric eel (Electrophorus electricus) made it one of the first model species in science. It was pivotal for understanding animal electricity in the 1700s, was investigated by Humboldt and Faraday in the 1800s, was leveraged to isolate the acetylcholine receptor in the 20th century, and has inspired the design of new power sources and provided insights to electric organ evolution in the 21st century. And yet few studies have investigated the electric eel's behavior. This review focuses on a series of recently discovered behaviors that evolved alongside the eel's extreme physiology. Eels use their high-voltage electric discharge to remotely control prey by transcutaneously activating motor neurons. Hunting eels use this behavior in two different ways. When prey have been detected, eels use high-voltage to cause immobility by inducing sustained, involuntary muscle contractions. On the other hand, when prey are hidden, eels often use brief pulses to induce prey twitch, which causes a water movement detected by the eel's mechanoreceptors. Once grasped in the eel's jaws, difficult prey are often subdued by sandwiching them between the two poles (head and tail) of the eel's powerful electric organ. The resulting concentration of the high-voltage discharge, delivered at high-rates, causes involuntary fatigue in prey muscles. This novel strategy for inactivating muscles is functionally analogous to poisoning the neuromuscular junction with venom. For self-defense, electric eels leap from the water to directly electrify threats, efficiently activating nociceptors to deter their target. The latter behavior supports a legendary account by Alexander von Humboldt who described a battle between electric eels and horses in 1800. Finally, electric eels use high-voltage not only as a weapon, but also to efficiently track fast-moving prey with active electroreception. In conclusion, remarkable behaviors go hand in hand with remarkable physiology.

How Not to Be Turned into a Zombie.

The emerald jewel wasp (Ampulex compressa) is renowned for its ability to zombify the American cockroach (Periplaneta americana) with a sting to the brain. When the venom takes effect, the cockroach becomes passive and can be led by its antenna into a hole, where the wasp deposits an egg and then seals the exit with debris. The cockroach has the ability to walk, run, or fly if properly stimulated, but it does not try to escape as it is slowly eaten alive by the developing wasp larva. Although the composition and effects of the wasp's venom have been investigated, no studies have detailed how cockroaches might prevent this grim fate. Here it is shown that many cockroaches deter wasps with a vigorous defense. Successful cockroaches elevated their bodies, bringing their neck out of reach, and kicked at the wasp with their spiny hind legs, often striking the wasp's head multiple times. Failing this, the elevated, "on-guard" position allowed cockroaches to detect and evade the wasp's lunging attack. If grasped, the cockroaches parried the stinger with their legs, used a "stiff-arm" defense to hold back the stinger, and could stab at, and dislodge, the wasp with tibial spines. Lastly, cockroaches bit at the abdomen of wasps delivering the brain sting. An aggressive defense from the outset was most successful. Thus, for a cockroach not to become a zombie, the best strategy is: be vigilant, protect your throat, and strike repeatedly at the head of the attacker.

Power Transfer to a Human during an Electric Eel's Shocking Leap.

Electric eels have been the subject of investigation and curiosity for centuries [1]. They use high voltage to track [2] and control [3] prey, as well as to exhaust prey by causing involuntary fatigue through remote activation of prey muscles [4]. But their most astonishing behavior is the leaping attack, during which eels emerge from the water to directly electrify a threat [5, 6]. This unique defense has reportedly been used against both horses [7] and humans [8]. Yet the dynamics of the circuit that develops when a living animal is contacted and the electrical power transmitted to the target have not been directly investigated. In this study, the electromotive force and circuit resistances that develop during an eel's leaping behavior were determined. Next, the current that passed through a human subject during the attack was measured. The results allowed each variable in the equivalent circuit to be estimated. Findings can be extrapolated to a range of different eel sizes that might be encountered in the wild. Despite the comparatively small size of the eel used in this study, electrical currents in the target peaked at 40-50 mA, greatly exceeding thresholds for nociceptor activation reported for both humans [9] and horses [10, 11]. No subjective sensation of involuntary tetanus was reported, and aversive sensations were restricted to the affected limb. Results suggest that the main purpose of the leaping attack is to strongly deter potential eel predators by briefly causing intense pain. Apparently a strong offense is the eel's best defense.

Electrical Potential of Leaping Eels.

When approached by a large, partially submerged conductor, electric eels (Electrophorus electricus) will often defend themselves by leaping from the water to directly shock the threat. Presumably, the conductor is interpreted as an approaching terrestrial or semiaquatic animal. In the course of this defensive behavior, eels first make direct contact with their lower jaw and then rapidly emerge from the water, ascending the conductor while discharging high-voltage volleys. In this study, the equivalent circuit that develops during this behavior was proposed and investigated. First, the electromotive force and internal resistance of four electric eels were determined. These values were then used to estimate the resistance of the water volume between the eel and the conductor by making direct measurements of current with the eel and water in the circuit. The resistance of the return path from the eel's lower jaw to the main body of water was then determined, based on voltage recordings, for each electric eel at the height of the defensive leap. Finally, the addition of a hypothetical target for the leaping defense was considered as part of the circuit. The results suggest the defensive behavior efficiently directs electrical current through the threat, producing an aversive and deterring experience by activating afferents in potential predators.

Comparative Morphology of the Penis and Clitoris in Four Species of Moles (Talpidae).

The penile and clitoral anatomy of four species of Talpid moles (broad-footed, star-nosed, hairy-tailed, and Japanese shrew moles) were investigated to define penile and clitoral anatomy and to examine the relationship of the clitoral anatomy with the presence or absence of ovotestes. The ovotestis contains ovarian tissue and glandular tissue resembling fetal testicular tissue and can produce androgens. The ovotestis is present in star-nosed and hairy-tailed moles, but not in broad-footed and Japanese shrew moles. Using histology, three-dimensional reconstruction, and morphometric analysis, sexual dimorphism was examined with regard to a nine feature masculine trait score that included perineal appendage length (prepuce), anogenital distance, and presence/absence of bone. The presence/absence of ovotestes was discordant in all four mole species for sex differentiation features. For many sex differentiation features, discordance with ovotestes was observed in at least one mole species. The degree of concordance with ovotestes was highest for hairy-tailed moles and lowest for broad-footed moles. In relationship to phylogenetic clade, sex differentiation features also did not correlate with the similarity/divergence of the features and presence/absence of ovotestes. Hairy-tailed and Japanese shrew moles reside in separated clades, but they exhibit a high degree of congruence. Broad-footed and hairy-tailed moles reside within the same clade but had one of the lowest correlations in features and presence/absence of ovotestes. Thus, phylogenetic affinity and the presence/absence of ovotestes are poor predictors for most sex differentiation features within mole external genitalia.

Behavioral pieces of neuroethological puzzles.

In this review, I give a first-person account of surprising insights that have come from the behavioral dimension of neuroethological studies in my laboratory. These studies include the early attempts to understand the function of the nose in star-nosed moles and to explore its representation in the neocortex. This led to the discovery of a somatosensory fovea that parallels the visual fovea of primates in several ways. Subsequent experiments to investigate the assumed superiority of star-nosed moles to their relatives when locating food led to the unexpected discovery of stereo olfaction in common moles. The exceptional olfactory abilities of common moles, in turn, helped to explain an unusual bait-collecting technique called "worm-grunting" in the American southeast. Finally, the predatory behavior of tentacled snakes was best understood not by exploring their nervous system, but rather by considering fish nervous systems. These experiences highlight the difficulty of predicting the abilities of animals that have senses foreign to the investigator, and also the rewards of discovering the unexpected.

Leaping eels electrify threats, supporting Humboldt's account of a battle with horses.

In March 1800, Alexander von Humboldt observed the extraordinary spectacle of native fisherman collecting electric eels (Electrophorus electricus) by "fishing with horses" [von Humboldt A (1807) Ann Phys 25:34-43]. The strategy was to herd horses into a pool containing electric eels, provoking the eels to attack by pressing themselves against the horses while discharging. Once the eels were exhausted, they could be safely collected. This legendary tale of South American adventures helped propel Humboldt to fame and has been recounted and illustrated in many publications, but subsequent investigators have been skeptical, and no similar eel behavior has been reported in more than 200 years. Here I report a defensive eel behavior that supports Humboldt's account. The behavior consists of an approach and leap out of the water during which the eel presses its chin against a threatening conductor while discharging high-voltage volleys. The effect is to short-circuit the electric organ through the threat, with increasing power diverted to the threat as the eel attains greater height during the leap. Measurement of voltages and current during the behavior, and assessment of the equivalent circuit, reveal the effectiveness of the behavior and the basis for its natural selection.

Somatosensory organ topography across the star of the star-nosed mole (Condylura cristata).

Quantifying somatosensory receptor distribution in glabrous skin is usually difficult because of the diversity of skin receptor subtypes and their location within the dermis and epidermis. However, the glabrous noses of moles are an exception. In most species of moles, the skin on the nose is covered with domed mechanosensory units known as an Eimer's organs. Eimer's organs contain a stereotyped array of different mechanosensory neurons, meaning that the distribution of mechanosensitive nerve endings can be inferred by visual inspection of the skin surface. Here we detail the distribution of Eimer's organs on the highly derived somatosensory star on the rostrum of the star-nosed mole (Condylura cristata). The star consists of 22 fleshy appendages, or rays, that are covered in Eimer's organs. We find that the density of Eimer's organs increases from proximal to distal locations along the length of the star's rays with a ratio of 1:2.3:3.1 from the surface nearest to the nostril, to the middle part of ray, to the ray tip, respectively. This ratio is comparable to the increase in receptor unit density reported for the human hand, from the palm, to the middle of the digits, to the distal fingertips. We also note that the tactile fovea of the star-nosed mole, located on the medial ventral ray, does not have increased sensory organ density, and we describe these findings in comparison with other sensory fovea.

Electric Eels Concentrate Their Electric Field to Induce Involuntary Fatigue in Struggling Prey.

Nature is replete with predator venoms that immobilize prey by targeting ion channels. Electric eels (Electrophorus electricus) take a different tactic to accomplish the same end. Striking eels emit electricity in volleys of 1 ms, high-voltage pulses. Each pulse is capable of activating prey motor neuron efferents, and hence muscles. In a typical attack, eel discharges cause brief, immobilizing tetanus, allowing eels to swallow small prey almost immediately. Here I show that when eels struggle with large prey or fish held precariously, they commonly curl to bring their own tail to the opposite side of prey, sandwiching it between the two poles of their powerful electric organ. They then deliver volleys of high-voltage pulses. Shortly thereafter, eels juggle prey into a favorable position for swallowing. Recordings from electrodes placed within prey items show that this curling behavior at least doubles the field strength within shocked prey, most likely ensuring reliable activation of the majority of prey motor neurons. Simulated pulse trains, or pulses from an eel-triggered stimulator, applied to a prey muscle preparations result in profound muscle fatigue and loss of contractile force. Consistent with this result, video recordings show that formerly struggling prey are temporarily immobile after this form of attack, allowing the manipulation of prey that might otherwise escape. These results reveal a unique use of electric organs to a unique end; eels superimpose electric fields from two poles, ensuring maximal remote activation of prey efferents that blocks subsequent prey movement by inducing involuntary muscle fatigue.

Electric eels use high-voltage to track fast-moving prey.

Electric eels (Electrophorus electricus) are legendary for their ability to incapacitate fish, humans, and horses with hundreds of volts of electricity. The function of this output as a weapon has been obvious for centuries but its potential role for electroreception has been overlooked. Here it is shown that electric eels use high-voltage simultaneously as a weapon and for precise and rapid electrolocation of fast-moving prey and conductors. Their speed, accuracy, and high-frequency pulse rate are reminiscent of bats using a 'terminal feeding buzz' to track insects. Eel's exhibit 'sensory conflict' when mechanosensory and electrosensory cues are separated, striking first toward mechanosensory cues and later toward conductors. Strikes initiated in the absence of conductors are aborted. In addition to providing new insights into the evolution of strongly electric fish and showing electric eels to be far more sophisticated than previously described, these findings reveal a trait with markedly dichotomous functions.

An Optimized Biological Taser: Electric Eels Remotely Induce or Arrest Movement in Nearby Prey.

Despite centuries of interest in electric eels, few studies have investigated the mechanism of the eel's attack. Here, I review and extend recent findings that show eel electric high-voltage discharges activate prey motor neuron efferents. This mechanism allows electric eels to remotely control their targets using two different strategies. When nearby prey have been detected, eels emit a high-voltage volley that causes whole-body tetanus in the target, freezing all voluntary movement and allowing the eel to capture the prey with a suction feeding strike. When hunting for cryptic prey, eels emit doublets and triplets, inducing whole-body twitch in prey, which in turn elicits an immediate eel attack with a full volley and suction feeding strike. Thus, by using their modified muscles (electrocytes) as amplifiers of their own motor efferents, eel's motor neurons remotely activate prey motor neurons to cause movement (twitch and escape) or immobilization (tetanus) facilitating prey detection and capture, respectively. These results explain reports that human movement is 'frozen' by eel discharges and shows the mechanism to resemble a law-enforcement Taser.