Hunting strategy of a generalist ant species proposed as a biological control agent against termites

We studied the hunting behaviour of Myrmicaria opaciventris (Hymenoptera: Formicidae) in order to evaluate if it can be used as a biological control agent against the termites that damage sugarcane plantations. Hunting workers foraged in groups and recruited nestmates at short-range when they encountered large termite soldiers or groups of small termite workers. Differences in prey capture concerned the: (1) means of detection (from a distance or by contact); (2) termite body part seized (small termites seized by the body; large termites by an appendage); (3) percentages of prey abandoned; and (4) use of venom. The sting of the workers is spatulated implying a topical application of the venom on the prey. Large termites were stretched by several workers whose adherence to the substrate is facilitated by well-developed arolia and claws on the legs while others spread venom on the body and carved it up. An adaptation to termite capture was noted with a distribution of tasks between the workers which subdued prey, and those which transported it. In the former case, the workers easily eliminated termite soldiers, successively attacked several termite workers and even captured new individuals while holding the first ones captured between their mandibles before retrieving them all at once. The remaining individuals were retrieved by the transporting workers. Given this particularly effective predatory strategy, we concluded that, under certain conditions, M. opaciventris can be used as a biological control agent against termites.     

Prey capture behavior in an arboreal African ponerine ant

I studied the predatory behavior of Platythyrea conradti, an arboreal ponerine ant, whereas most species in this subfamily are ground-dwelling. The workers, which hunt solitarily only around dusk, are able to capture a wide range of prey, including termites and agile, nocturnal insects as well as diurnal insects that are inactive at that moment of the Nyctemeron, resting on tree branches or under leaves. Prey are captured very rapidly, and the antennal palpation used by ground-dwelling ponerine species is reduced to a simple contact; stinging occurs immediately thereafter. The venom has an instant, violent effect as even large prey (up to 30 times the weight of a worker) never struggled after being stung. Only small prey are not stung. Workers retrieve their prey, even large items, singly. To capture termite workers and soldiers defending their nest entrances, ant workers crouch and fold their antennae backward. In their role as guards, the termites face the crouching ants and end up by rolling onto their backs, their legs batting the air. This is likely due to volatile secretions produced by the ants' mandibular gland. The same behavior is used against competing ants, including territorially-dominant arboreal species that retreat further and further away, so that the P. conradti finally drive them from large, sugary food sources.     

Selection and capture of prey in the African ponerine antPlectroctena minor (Hymenoptera: Formicidae)

Prey selection by Plectroctena minor workers is two-fold. During cafeteria experiments, the workers always selected millipedes, their essential prey, while alternative prey acceptance varied according to the taxa and the situation. Millipedes were seized by the anterior part of their body, stung, and retrieved by single workers that transported them between their legs. They were rarely snapped at, and never abandoned. When P. minor workers were confronted with alternative prey they behaved like generalist species: prey acceptance was inversely correlated to prey size. This was not the case vis-à-vis millipedes that they selected and captured although larger than compared alternative prey. The semi-specialised diet of P. minor permits the colonies to be easily provisioned by a few foraging workers as millipedes are rarely hunted by other predatory arthropods, while alternative prey abound, resulting in low competition pressure in both cases. Different traits characteristic of an adaptation to hunting millipedes were noted and compared with the capture of alternative prey. We also noted the parsimony of the behavioural phases during their capture compared to the capture of alternative prey.     

Predatory Behavior in Dominant Arboreal Ant Species: The Case of Crematogaster sp. (Hymenoptera: Formicidae)

Crematogaster sp. is a dominant arboreal ant species that captures and retrieves very large prey. Hunting workers forage collectively thanks to short-range recruitment. They detect prey by contact, then rapidly attack, seizing small prey by the body and large prey by a leg. In this study, almost all the active prey were spread-eagled by several workers, even when small enough to permit a single worker to easily master them. While certain workers spread-eagled the prey, others deposited venom on the prey body using their spatulated sting (topical action of the venom). The well-developed arolia on the pretarsus of workers' legs have crucial importance for the success of prey capture (spread-eagling) and transport in an arboreal habitat. These results are compared with those known for other arboreal-dwelling generalist predator ant species.     

On the function of the ultimate legs of some Scolopendridae (Chilopoda,Scolopendromorpha)

The function of the variously shaped ultimate legs of Scolopendridae is briefly reviewed. Their function in Scolopendra heros Girard, 1853, Scolopendra subspinipes Leach, 1815, Scolopendra morsitans (Linnaeus, 1758), Scolopendra galapagoensis Bollman, 1889, Scolopendra hainanum Kronmüller, 2012, Scolopendra spinosissima Kraepelin, 1903 Cormocephalus aurantiipes (Newport, 1844) and Ethmostigmus trigonopodus (Leach, 1817), in which they are least specialised has been investigated. Specimens were tapped with forceps on different parts of the trunk to simulate the attack of a predator. When tapped on the first third of the trunk (near the head), the centipedes attacked the forceps with their forcipules. When tapped on the last third or the ultimate legs, they adopted a warning position, raising the ultimate legs to display the ventral and medial prefemoral spines as well as the spined coxopleural processes. In some cases the centipedes attacked the forceps with the claws of the ultimate legs by chopping down on them after lifting the legs high into the warning position. When tapped in the mid part of the trunk, the centipedes curled sideways to reach the forceps with their forcipules and ultimate legs simultaneously. Scolopendra galapagoensis not only lifted the ultimate legs into the warning position but also the last 3-4 pairs of locomotory legs, presenting their distodorsal prefemoral spines. This resembles the warning posture of some spiders. In addition to their function in warning behaviour, defensive stabbing, ritualised meeting reactions and during courtship behaviour, the ultimate legs may in addition act as hooks and perhaps be involved in species recognition. No evidence was found that the ultimate legs are used to catch prey, nor of prey or predators being held between the prefemora.     

Variable segment number in centipedes: population genetics meets evolutionary developmental biology

The case studies of population genetics focus on intraspecific variation, but most cases--at least where the variation is polymorphic--deal with characters that are not directly linked to organismic structure or ontogeny. Conversely, the case studies of evolutionary developmental biology focus directly on structure/ontogeny, but usually involve only interspecific comparisons. To integrate these complementary approaches, it is desirable to have a model system that permits study of intraspecific variation in development, using a character whose genetic basis either is already known or can be elucidated. Segment number in geophilomorph centipedes is proposed as a possible model system of this kind. Segment number is variable in natural populations of geophilomorphs, while in the other centipede orders it is fixed, either completely (scutigeromorphs, lithobiomorphs), or at least within species (scolopendromorphs). Statistical analysis of data on the extent of variation in different geophilomorph species suggests that segment number may be of selective importance, rather than the variation being merely an inevitable consequence of the difficulty of achieving a high degree of repeatability when there is a large number of segments.     

Wasp venom blocks central cholinergic synapses to induce transient paralysis in cockroach prey

The parasitoid wasp Ampulex compressa induces a set of unique behavioral effects upon stinging its prey, the cockroach. It stings into the first thoracic segment inducing 2 to 3 min of transient flaccid paralysis of the front legs. This facilitates a second sting in the cockroach's head that induces 30 min of excessive grooming followed by a 2 to 5-week long lethargic state. In the present study, we examine the immediate effect of the first sting, which is a transient paralysis of the front legs. Using radiolabeled wasps, we demonstrate that the wasp injects its venom directly into the cockroach's first thoracic ganglion. The artificial injection of milked venom into a thoracic ganglion abolishes spontaneous and evoked responses of the motoneurons associated with leg movements. To investigate the physiological mechanism of action of the venom, we injected venom into the last abdominal ganglion of the cockroach, which houses a well-characterized cholinergic synapse. Injected venom abolishes both sensory-evoked and agonist-evoked postsynaptic potentials recorded in the postsynaptic neuron for 2 to 3 min without affecting action potential propagation. Thus, the venom blocking effect has a postsynaptic component that follows the same time course as the transient paralysis induced by the thoracic sting. Finally, injection of a nicotinic antagonist in the front thoracic ganglion induces paralysis of the front legs. We conclude that the transient paralytic effect of the thoracic sting can be mainly accounted for by the presence of a venom active component that induces a postsynaptic block of central cholinergic synaptic transmission.     

THE RECOGNITION AND TREATMENT OF VENOMOUS AND NON-VENOMOUS INSECTS BY SMALL BEE-EATERS

The manner in which bee-eaters cope with the stinging honey-bees which comprise their principal food was investigated by aviary studies of Merops bullocki. Worker Apis are de-venomed by an innate sequence of beating the insect and rubbing its abdomen against the perch. Treatment improves with experience. Drone bees are distinguished by the birds from workers but are not instantly recognised as non-venomous; they are subjected to low intensity rubbing combined with non-venomous prey treatment concomitant with their size. Non-Hymenoptera, including some insects which superficially resemble bees, are recognised as non-venomous and are not rubbed, but are beaten until immobilized. Bee-eaters appear to have partial immunity to venom.     

Mandible strike: the lethal weapon of Odontomachus opaciventris against small prey

In order to study both the hunting efficiency and the flexibility of their predatory behavior, solitary hunters of the trap-jaw ant Odontomachus opaciventris were offered small prey (termites, fruit flies and tenebrionid larvae), presenting different morphological or defensive characteristics. The monomorphic hunters showed a moderately flexible predatory behavior characterized by short capture sequences and a noteworthy efficiency of their mandible strike (76.7-100% of prey retrievals), even when presented with Nasutitermes soldiers. Contrary to most poneromorph ants, antennal palpation of the prey before the attack was always missing, no particular targeted region of the prey's body was preferred, and no 'prudent' posture was ever exhibited. Moreover, stinging was regularly performed on bulky, fast moving fruit flies, very scarcely with sclerotized tenebrionid larvae, but never occurred with Nasutitermes workers or soldiers despite their noxious chemical defense. These results suggest that, whatever the risk linked to potentially dangerous prey, O. opaciventris predatory strategy optimizes venom use giving top priority to the swiftness and strength of the lethal trap-jaw system used by hunters as first strike weapon to subdue rapidly a variety of small prey, ranging from 0.3 to 2 times their own body size and from 0.1 to 2 times their weight. Such risk-prone predatory behavior is likely to be related to the large size of O. opaciventris colonies where the death of a forager might be of lesser vital outcome than in small colony-size species.     

Venom regeneration in the centipede Scolopendra polymorpha: evidence for asynchronous venom component synthesis

Venom regeneration comprises a vital process in animals that rely on venom for prey capture and defense. Venom regeneration in scolopendromorph centipedes likely influences their ability to subdue prey and defend themselves, and may influence the quantity and quality of venom extracted by researchers investigating the venom's biochemistry. We investigated venom volume and total protein regeneration during the 14-day period subsequent to venom extraction in the North American centipede Scolopendra polymorpha. We further tested the hypothesis that venom protein components, separated by reversed-phase fast protein liquid chromatography (RP-FPLC), undergo asynchronous (non-parallel) synthesis. During the first 48 h, volume and protein mass increased linearly. Protein regeneration lagged behind volume regeneration, with 65–86% of venom volume and 29–47% of protein mass regenerated during the first 2 days. No additional regeneration occurred over the subsequent 12 days, and neither volume nor protein mass reached initial levels 7 months later (93% and 76%, respectively). Centipede body length was negatively associated with rate of venom regeneration. Analysis of chromatograms of individual venom samples revealed that 5 of 10 chromatographic regions and 12 of 28 peaks demonstrated changes in percent of total peak area (i.e., percent of total protein) among milking intervals, indicating that venom proteins are regenerated asynchronously. Moreover, specimens from Arizona and California differed in relative amounts of some venom components. The considerable regeneration of venom occurring within the first 48 h, despite the reduced protein content, suggests that predatory and defensive capacities are minimally constrained by the timing of venom replacement.     

Prey orientation and the role of venom availability in the predatory behaviour of the centipede Scolopendra subspinipes mutilans (Arthropoda: Chilopoda)

Many animal phyla contain clades in which most or all species are venom-injecting predators. An example, in the arthropods, is the class Chilopoda, containing the approximately 3500 species of centipedes. Very little ecological or behavioural work yielding quantitative data has been conducted on centipede predation. Here, we describe a study of this kind. Our experiments employed one centipede species - a large tropical one, Scolopendra subspinipes mutilans - and two species of prey - a cricket, Gryllus assimilis, and a locust, Schistocerca gregaria. We conducted two experiments. The first was aimed at investigating the extent to which the centipedes attacked prey in particular tagmata as opposed to at random over the whole body surface. The results showed that the centipedes were highly selective, preferring to attack the head or thorax rather than the abdomen; indeed, they often reoriented the prey in order to achieve this. A possible explanation of this behaviour is to maximize the speed with which the neurotoxins in the venom reach either the brain or the thoracic ganglia that control limb movement. The second experiment was aimed at investigating the effect of venom-extraction on the attack rate, and specifically at testing if the magnitude of any such effect differed between the two types of prey, which differ considerably in size. The results showed a major effect of venom extraction in relation to both types of prey, but with the time taken to return to a 'normal' attack rate being longer in the case of the larger prey-type, namely the locust. We discuss these results in relation to the 'venom optimization hypothesis' and, more generally, to the principle of minimizing the production/use of venom, which is an energetically expensive resource.     

Venom spraying inParachartergus colobopterus: A novel defensive behavior in a social wasp (Hymenoptera: Vespidae)

Colonies ofParachartergus colobopterus do not defend against vertebrates by attacking and stinging. Instead, defending workers bend the gaster forward and spray a fine mist of venom in the direction of nearby moving objects. Although venom spraying has been reported forP. fraternus, a species that does sting, we found that this occurred only during sting attempts. We conclude that defensive behavior inP. colobopterus is unique among wasps in that (1) venom is sprayed at intruders by workers standing on the nest and (2) the spray is an atomized mist rather than a stream. We suggest that nest crypticity restricts vertebrate predators on this wasp to small, insect gleaning birds, against which a spray of venom in the eyes, mouth, and nasal passages is more effective than is a stinging defense.     

Cnidarian internal stinging mechanism

Stinging mechanisms generally deliver venomous compounds to external targets. However, nematocysts, the microscopic stinging organelles that are common to all members of the phylum Cnidaria, occur and act in both external and internal tissue structures. This is the first report of such an internal piercing mechanism. This mechanism identifies prey items within the body cavity of the sea anemone and actively injects them with cytolytic venom compounds. Internal tissues isolated from sea anemones caused the degradation of live Artemia salina nauplii in vitro. When examined, the nauplii were found to be pierced by discharged nematocysts. This phenomenon is suggested to aid digestive phagocytic processes in a predator otherwise lacking the means to masticate its prey.     

Bugs with a backpack: the function of nymphal camouflage in the West African assassin bugs Paredocla andAcanthaspis spp.

The nymphs of the West African assassin bugs Paredocla and Acanthaspis spp. disguise themselves with a cover of dust, sand and soil particles (‘dust coat’) and additionally pile a ‘backpack’ of larger objects, such as empty prey corpses and plant parts, on their abdomen. We investigated the effect of this conspicuous camouflage in interactions of the bugs with ants, their main prey, as well as in encounters with their own predators. Experiments with three ant species showed that the dust coat impedes chemical and tactile recognition of the nymphs by ant workers and thus may serve to increase their hunting success. The backpack appeared to play only a minor role in this context. In arena experiments with three potential predators (spiders, geckos and centipedes), camouflaged nymphs were significantly more likely to survive than denuded bugs. Here the observed effect was mainly attributable to the backpack, which enhanced the concealing effect of the dust coat and confused visually orienting predators. In addition, in the case of an attack, it could be shed to distract the enemy while the bug escaped, thus functioning in a similar manner as a lizard’s tail.     

Intraspecies variability and conopeptide profiling of the injected venom of Conus ermineus

The venom of cone snails (ssp. Conus), a genus of predatory mollusks, is a vast source of bioactive peptides. Conus venom expression is complex, and venom composition can vary considerably depending upon the method of extraction and the species of cone snail in question. The injected venom from Conus ermineus, the only fish-hunting cone snail species that inhabits the Atlantic Ocean, was characterized using nanoNMR spectroscopy, MALDI-TOF mass spectrometry, RP-HPLC and nanoLC-ESI-MS. These methods allowed us to evaluate the variability of the venom within this species. Single specimens of C. ermineus show unchanged injected venom mass spectra and HPLC profiles over time. However, there was significant variability of the injected venom composition from specimen to specimen, in spite of their common biogeographic origin. Using nanoLC-ESI-MS, we determined that over 800 unique conopeptides are expressed by this reduced set of C. ermineus specimens. This number is considerably larger than previous estimates of the molecular repertoire available to cone snails to immobilize prey. These results support the idea of the existence of a complex regulatory mechanism to express specific venom peptides for injection into prey. These intraspecies differences can be a result of a combination of genetic and environmental factors. The differential expression of venom components represents a neurochemical paradigm that warrants further investigation.     

Arboreal Ants Use the “Velcro? Principle” to Capture Very Large Prey

Plant-ants live in a mutualistic association with host plants known as “myrmecophytes” that provide them with a nesting place and sometimes with extra-floral nectar (EFN) and/or food bodies (FBs); the ants can also attend sap-sucking Hemiptera for their honeydew. In return, plant-ants, like most other arboreal ants, protect their host plants from defoliators. To satisfy their nitrogen requirements, however, some have optimized their ability to capture prey in the restricted environment represented by the crowns of trees by using elaborate hunting techniques. In this study, we investigated the predatory behavior of the ant Azteca andreae which is associated with the myrmecophyte Cecropia obtusa. We noted that up to 8350 ant workers per tree hide side-by-side beneath the leaf margins of their host plant with their mandibles open, waiting for insects to alight. The latter are immediately seized by their extremities, and then spread-eagled; nestmates are recruited to help stretch, carve up and transport prey. This group ambush hunting technique is particularly effective when the underside of the leaves is downy, as is the case for C. obtusa. In this case, the hook-shaped claws of the A. andreae workers and the velvet-like structure of the underside of the leaves combine to act like natural Velcro® that is reinforced by the group ambush strategy of the workers, allowing them to capture prey of up to 13,350 times the mean weight of a single worker.     

Coevolution of diet and prey-specific venom activity supports the role of selection in snake venom evolution

The processes that drive the evolution of snake venom variability, particularly the role of diet, have been a topic of intense recent research interest. Here, we test whether extensive variation in venom composition in the medically important viper genus Echis is associated with shifts in diet. Examination of stomach and hindgut contents revealed extreme variation between the major clades of Echis in the proportion of arthropod prey consumed. The toxicity (median lethal dose, LD₅₀) of representative Echis venoms to a natural scorpion prey species was found to be strongly associated with the degree of arthropod feeding. Mapping the results onto a novel Echis phylogeny generated from nuclear and mitochondrial sequence data revealed two independent instances of coevolution of venom toxicity and diet. Unlike venom LD₅₀, the speed with which venoms incapacitated and killed scorpions was not associated with the degree of arthropod feeding. The prey-specific venom toxicity of arthropod-feeding Echis may thus be adaptive primarily by reducing venom expenditure. Overall, our results provide strong evidence that variation in snake venom composition results from adaptive evolution driven by natural selection for different diets, and underscores the need for a multi-faceted, integrative approach to the study of the causes of venom evolution.     

Wasp uses venom cocktail to manipulate the behavior of its cockroach prey

The sting of the parasitoid wasp Ampulex compressa is unusual, as it induces a transient paralysis of the front legs followed by grooming behavior and then by a long-term hypokinesia of its cockroach prey. Because the wasp's goal is to provide a living meal for its newborn larva, the behavioral changes in the prey are brought about by manipulating the host behavior in a way beneficial to the wasp and its offspring. To this end, the wasp injects its venom cocktail with two consecutive stings directly into the host's central nervous system. The first sting in the thorax causes a transient front leg paralysis lasting a few minutes. This paralysis is due to the presence of a venom component that induces a postsynaptic block of central cholinergic synaptic transmission. Following the head sting, dopamine identified in the venom appears to induce 30 min of intense grooming. During the long-term hypokinesia that follows the grooming, specific behaviors of the prey are inhibited while others are unaffected. We propose that the venom represses the activity of head ganglia neurons thereby removing the descending excitatory drive to the thoracic neurons.Abbreviations CNS central nervous system - DA dopamine - GI giant interneuron - PSP postsynaptic potential - SEG sub-esophageal ganglion - TI thoracic interneuron     

Differences in venom and cuticular peptides in individuals of Apis mellifera (Hymenoptera: Apidae) determined by MALDI-TOF MS

The fraction between 950 and 4000 Da of the venom of Apis mellifera has been analyzed with MALDI-TOF mass spectrometry and statistical facilities of the ClinProTools™ software. Consistent differences in the composition of this venom fraction were observed between queens and workers while younger and older workers (nurses and guards as well as foragers) differ for the relative percentages of two well known cytolytic peptides, namely Melittin and Apamin. Total in situ body methanol extracts and methanol micro-extractions on the cuticle of various parts of the body of drones and females confirmed that venom peptides are smeared on the body surface of females in a not yet clarified way. The observation that venom peptides have been found also on comb wax rises the hypothesis that the use of venom as antimicrobial agent makes part of the social immunity system of A. mellifera.