Ovipositor

Egg-Laying

Most female crickets inject their eggs into the soil or into plant stems through long, slender ovipositors. The oviposition slashes of tree crickets often seriously damage berry canes and small twigs. Females of the two subterranean subfamilies do not inject their eggs into the soil and have lost the external ovipositor; a few Brachytrupinae retain short ovipositors and inject eggs shallowly into burrow walls. Most subterranean forms lay only a few eggs in one place in an underground chamber. In those studied, such as the North American species Anurogryllus arboreus, plant materials are also stored in the burrow, and a special defecation chamber is excavated; juveniles eat stored plant materials, small unfertilized eggs produced by the mother after the young hatch, and eventually the body of the dead mother. A female may dig her own burrow or ferociously take over and defend the burrow of a courting male before allowing him to mate with her at the entrance.

The Ovipositor: A Key Organ

Since Hymenoptera in general are known to take great care in the placement of their eggs, it is not surprising that the ovipositor is an important organ, and one that has shown many specializations for particular modes of life.

The hymenopteran ovipositor is derived from abdominal appendages and comprises three independently movable parts, called valves, that together form the egg canal. The dorsal valve is a fused structure, but the ventral ones are separate. There is no intrinsic ovipositor musculature; rather, the movements of the valves depend on muscles within the abdomen that pull on the internal apodemes of the three valves. Nevertheless, several parasitic taxa have evolved mechanisms that enable them to steer their ovipositors and thus increase their chances of successfully attacking a mobile host that might otherwise be able to wriggle away from its attacker. Although the penetration of the substrate by wasp ovipositors is usually referred to as “drilling,” it is important to realize that there is no circular motion: penetration is achieved by the to-and-fro motion of the three valves relative to one another. In the simplest mode of operation, one valve has a projection or nodus that interlocks with the substrate, and this acts as a support for the others to be pushed forward.

The sawflies get their name from the laterally compressed, strongly serrated, ovipositors with which they insert their eggs under plant cuticle. These ovipositors are unsuited, however, for penetration of wood, and the wood wasps’ ovipositors are longer and rounder in cross section, with serrations used for rasping wood fibers, located just at the tip (see Fig. 2). Most of the parasitic Hymenoptera have a similar ovipositor except that in many of those with exposed hosts it is much shorter and has reduced serrations because there is no substrate to “drill” through. Some ovipositors are very long (up to 12 times longer than the wasp's body), and various mechanisms and behaviors have evolved to enable the wasp to manipulate them.

Figure 2. A large ichneumonid wasp, Megarhyssa sp., using its ovipositor to “drill” through a tree trunk to reach its host, a siricid wood wasp larva. The ovipositor is very thin and pointing between the fore legs; the large black structures are the protective ovipositor sheaths.

(Photograph by Nathan Schiff.)

Behavior and Interactions

Mechanism of Action

There are numerous variations in the venom apparatus of members of Hymenoptera (Fowler, 1993). The stinger is a modification of the ovipositor apparatus and is found only in female bees and wasps. Venom secreted from specialized cells in the acid glands is transported to the venom sac reservoir via small tubules. One-way valves in the bulb of the venom apparatus control the flow of venom during envenomation. At the time of venom injection, the alkaline gland contributes a secretion that enhances the toxicity of the venom. The stinger of the honeybee is covered with retrograde barbs that cause the stinger to remain impaled in thick-skinned victims. When this occurs and the bee attempts to withdraw, the entire stinger apparatus is pulled from the bee, resulting in death of the honeybee.

Honeybee venoms are complex mixtures of proteins, peptides, and small organic molecules (Akre and Reed, 2002). Phospholipases and hyaluronidases present in the venom account for the majority of allergic responses to bee venoms in humans and likely other animals as well. Phospholipase A₂ is one of the most lethal peptides in honeybee venom (Schmidt, 1995). Mellitin is a membrane disruptive compound that increases the susceptibility of cell membranes to the damage caused by phospholipases within the venom (Akre and Reed, 2002). Mellitin can also cause pain, trigger hemolysis, increase capillary blood flow, increase cell permeability, and enhance spread of venom constituents within tissue. Mellitin, in combination with phospholipase and a mast cell degranulating peptide, triggers the release of histamine and serotonin. In mice, mellitin was found to be the primary lethal component of honeybee venom (Schmidt, 1995). Apamin is a neurotoxin that blocks calcium-activated potassium channels and has been associated with transient peripheral nerve effects in humans after bee stings (Saravanan et al., 2004). In cats, bee venom can cause contraction of bronchiolar muscles.

Like honeybees, vespid wasps (including yellow jackets and hornets) produce venoms containing peptides, enzymes, and amines designed to trigger pain (Akre and Reed, 2002). The primary pain-inducing substances are kinins; however, other compounds present in vespid venom, such as serotonin, histamine, tyramine, catecholamines, and acetylcholine, can contribute to the pain as well as local vasoactivity. Several of the constituents of vespid venom can act as allergens and trigger allergic reactions. Some vespid venoms contain neurotoxins or alarm pheromones that alert the swarm to an intruder.

Sources

The stinging insects are members of the order Hymenoptera of the class Insecta. These venomous insects possess the capability to sting using a modified ovipositor found on the terminal end of their abdomen. The three medically important groups are the Apoidea (bees—with 20,000 species), Vespoidea (the wasps, hornets, and yellow jackets—with 15,000 species) and Formicidae (the ants—with 15,000 species). The fire ants will be considered separately in this discussion.

The family Apoidae includes the social honeybees, the solitary bees, and bumblebees. Honeybees are herbivorous and live on nectar and pollen. Wasps, hornets, and yellow jackets (Vespoidae) are predaceous carnivores and live on other insects and sweet substances, such as sap and nectar. Feeding cues for bees emanate from flowers among which they forage. The feeding cue for the vespids comes from flesh and the smell of sugars. There is often a great deal of misidentification between bees and their vespid cousins. However, the two groups differ tremendously in their behavior and body type and can be readily identified. Honeybees are social insects and build their nests (hives) in hollow trees or other cavities. Yellow jackets are usually ground dwellers, whereas the hornets and wasps live in shrubs and trees, and are not ground nesting. Unlike bees, vespids can be frequently found near open cans of soft drinks and sweet food and garbage.

The stinger of these insects is another method of identification.^1,2 Honeybees can only sting once; they possess a barbed stinger that stays behind in the victim's skin after they sting. The stinger and the venom sac are pulled out of the bee's abdomen and soon after the insect dies. Wasp, hornet, and yellow jacket stingers are not barbed and each insect is capable of delivering multiple venom-injecting stings without dying.³ Vespids are much more aggressive while bees are generally more docile. However, honeybees will vigorously defend their hives against intruders. Typically, people and animals are stung accidentally when they step on bees or otherwise disturb the insects. An exception to this is the aggressive behavior of the more recently introduced Africanized honeybee. These bees attack more readily than their European and North American counterparts, potentially inflicting hundreds of stings.⁴ If the offending specimen causing the sting is not available, learning the circumstances of the stinging incident, looking for the presence of a stinger in a victim, knowing the differences in body types, and understanding the behavioral differences between bees and wasps can be instrumental in correctly identifying the stinging insect.⁵ The taxonomy and relationship of hymenopterans is illustrated in Figure 48-1.

THE CARBONIFEROUS (362–290 MYA)

The Carboniferous period is famous for the wet, warm climates and extensive swamps of mosses, ferns, seed ferns, horsetails, and calamites. Remains of insects are scattered throughout Carboniferous coal deposits (particularly blattarian wings); two particularly important deposits are Mazon Creek, Illinois, and Commentry, France. The earliest pterygotes appear in the Carboniferous, including the Blattaria, †Caloneurodea, primitive stem-group ephemeropterans (Fig. 4F), Orthoptera, †Paleodictyopteroidea (Figs. 4C and 4D), †“Protodonata” (Fig. 4E), and †”Protorthoptera”; the latter two are paraphyletic assemblages of primitive pterygotes.

Hypotheses on the evolution of insect wings include their use originally as gills or gill covers, or for mating displays, but early outgrowths of the insect pleuron most plausibly served in gliding. Feeding damage on plants is also recorded first in the Carboniferous, in the form of punctures and deep holes probably made by the long, beaked mouthparts of paleodictyopteroid insects. Thus, insects have been evolving in close association with plants for at least 350 million years, which is longer than any other group of terrestrial animals. Arborescent plants appear in the Upper Devonian, and as Carboniferous insects increasingly dwelled in them to feed, gliding probably became so adaptive for escape and dispersal that flapping wings and powered flight evolved rather suddenly.

Putative Holometabola are recorded from the Carboniferous. One is a larva from Mazon Creek, Srokalarva berthei, many features of which are inconsistent with extant holometabolan larvae, including segmented abdominal legs, ocelli, and possible compound eyes. Legs and body segments of Srokalarva are undifferentiated, as in myriapods. Some tree fern galls (ca. 300 mya) are attributed to the Holometabola on the basis of size of frass pellets in the galls. Some Paleozoic arthropods were considerably larger than living relatives, and Carboniferous gall-making mites are also known, and so it is possible that large mites caused these ancient galls. The earliest definitive Holometabola occur in the Permian.

4.3.3 Host–Parasitoid Interactions

Unlike hymenopterans, dipteran parasitoids cannot suppress the host immune system or affect host physiology through secretions injected by ovipositing females (dipteran parasitoids lack a “true” piercing ovipositor) or derived from teratocytes. Yet, dipteran parasitoids display good strategies, which are especially known for tachinids, to avoid host encapsulation. Many tachinid larvae escape the host immune response and turn the host response to their advantage by forming respiratory funnels, which are sclerotized folders around the hind part of their body. Funnels may be primary, built in the host integument by first instars as soon as they enter, or secondary, formed by late-first or early-second instars in the host integument or tracheae. The tachinids that form primary funnels (E. larvarum) breathe atmospheric air from the beginning of their development, which permits them to grow rapidly, while those forming secondary funnels (E. bryani and P. rufifrons) breathe through their integument, and thus grow slowly, until funnel formation. The early larval stages of the tachinids that do not form primary funnels may escape host immune response by moving into a specific host tissue, such as muscle (P. rufifrons), or between the peritrophic membrane and gut wall (C. concinnata) (Baronio and Campadelli, 1979; Ichiki and Shima, 2003).

Another interesting aspect is host development following parasitoid attack. Parasitoids may be classified as “koinobionts” or “idiobionts”; koinobionts allow their host to continue to feed and grow beyond parasitization, whereas idiobionts permanently paralyze or kill the host before the parasitoid egg hatches (Haeselbarth, 1979; Askew and Shaw, 1986). However, dipteran parasitoids do not fit well into this classification. Many species show characteristics of both strategies, for example tachinids (Dindo, 2011) and bombyliids (Yeates and Greathead, 1997). In Tachinidae, many species (P. rufifrons, Pseudoperichaeta nigrolineata, and A. marmoratus) exhibit a high degree of physiological integration with their host. The development of these species is dependent on host hormones because their first-instar larvae have to wait until the host larva has reached maturity or is in the pupal stage before molting to second instar (Baronio and Sehnal, 1980; Grenier, 1988b). As a consequence, the duration of their larval development is widely influenced by host age at parasitization (Mellini, 1986). Other tachinid (and also sarcophagid) parasitoids do not show a developmental synchrony with their host and develop continuously until pupation. These species, especially those that form primary integumental respiratory funnels (E. larvarum), grow quickly following attack and kill the host rapidly, thereby behaving as zoonecrophages for most of their larval life. The degree of complexity of host–parasitoid interaction and the extent of host development following attack are related not only to developmental synchrony but also to respiration strategies. In fact, the tachinids that do not depend on host hormones, but form secondary funnels, grow continuously until pupation and keep the host alive longer than those building primary funnels. For E. bryani and C. concinnata, host–parasitoid interactions have also been found to be widely influenced by host age at parasitization (Coulibaly and Fanti, 1992; Caron et al., 2010).

Belshaw (1994) suggested that, similar to hymenopteran parasitoids, tachinids exhibiting a complex life history are generally less polyphagous than those that display rapid development. However, there are tachinids with a relatively narrow host range despite their independence from host hormones (P. sylvestris), whereas a high level of polyphagy is shown by a number of species displaying complicated host–parasitoid interactions (C. concinnata) (Godwin and Odell, 1984). In tachinids, polyphagy seems to be connected to the parasitoid’s ability to avoid the host encapsulation response and/or indirect oviposition strategies (Askew and Shaw, 1986). In vivo production of species with a complex life history (whether based on respiration mode or hormonal interactions with the host) is not necessarily complicated, even on factitious hosts. For instance, the larval–pupal parasitoid P. rufifrons has successfully been cultured for many years in laboratory conditions on its factitious host Galleria mellonella (L.) (Mellini and Coulibaly, 1991). In contrast, host–parasitoid relationships may deeply influence the success of in vitro culture because tachinids exhibiting developmental synchrony with the host are known to be difficult to rear on artificial media (Dindo, 1998; Thompson, 1999). Independent of hormonal interactions, respiration adaptations of the parasitoid larvae have considerable impact on methods of in vitro rearing. Species that build primary funnels need to stay in contact with air from the first instar, which makes liquid media unsuitable for their culture. In vitro development may be more problematic for parasitoids that induce the formation of secondary, rather than primary, funnels (Dindo, 2011).

Aspects related to host–parasitoid interactions are known for only a few cryptochaetid species, such as C. iceryae (gregarious) and C. grandicorne (solitary). The larvae of these endoparasitoids do not build respiratory funnels but breathe through two caudal filaments containing tracheae, which become entangled with the host tracheae. Pupation may occur inside or outside the host scale carcass.

The host–parasitoid interactions displayed by Pseudacteon phorids with their fire ant hosts are rather complex and peculiar. The fly larvae develop and build respiratory structures in the head capsule of the host ant, which displays altered behavior and is finally decapitated. Larvae turn into pupae within the detached head capsule (Porter, 1998; Mathis and Philpott, 2012). Due to this manner of pupation and difficulties involved in the collection of fertilized eggs, in vitro rearing of Pseudacteon would be difficult to obtain on a large scale (Vogt et al., 2003). Conversely, sarcophagids attacking advanced larval stages or pupae of lepidopterans, such as A. housei and Agria affinis (Fallen), behave as zoosaprophages for most of their development and therefore show simple host–parasitoid interactions. Because of this characteristic, A. housei was successfully reared in vitro for many generations on different types of media (House and Traer, 1949).

3.12.3.1 Major Functions

In insects, chordotonal organs are found in all major body regions (head, thorax, abdomen) and many appendages (antennae, mouthparts, legs, wings, ovipositors, cerci). Modalities include joint proprioception (connective chordotonal organs), substrate vibration (subgenual organs), sound (tympanal organs) (Field, L. H. and Matheson, T., 1998), and infrared detection in the fire beetle (Mainz, T. et al., 2004). Some organs are broadly homologous in many different species, such as the femoral chordotonal organ that detects femur–tibial movements and is involved in control of the leg musculature (Moran, D. T. et al., 1975; Field, L. H. and Matheson, T., 1998; DiCaprio, R. A. et al., 2002), and Johnston’s organ in the pedicel (second segment) of insect antenna (McIver, S. B., 1985). Johnston’s organs contains both type 1 and type 2 sensilla but they always terminate in one tube (amphinematic) ending. Johnston’s organ is prominent in Diptera, with up to 20 000 sensory neurons in each male mosquito antenna, where they detect the sound produced by female mosquito wings (McIver, S. B., 1985).