Hemipepsis ustulata

The tarantula hawk's namesake comes from its predation of tarantulas to raise their young. After mating, the female wasp seeks out a tarantula, either free-ranging or in its burrow. After grappling with the tarantula, the wasp delivers a powerful sting that essentially paralyzes the tarantula permanently, but keeps it alive.[2] This allows the wasp to lay an egg that adheres to the spider's abdomen. One tarantula is provisioned per egg. The egg is about 5 mm long, gently curved, and creamy white in color. The wasp then drags the paralyzed tarantula along with the egg, sometimes up to 100 m, to a cavity or burrow to be sealed.[5] This dugout can be either dug by the wasp or be the burrow of the paralyzed spider.[6] When the larva hatches, it feeds on the spider's guts to completion, keeping the spider alive for as long as possible for freshness.[7]

About three days after the egg is laid, the free end of the egg becomes glassy white. The grub chews its way out with its tiny, dark-tipped mandibles. Eventually, the eggshell splits, revealing the glistening, white, footless grub. The grub, still attached to the host tarantula by its tail end, arches over and digs into the tarantula's skin, creating a perforation aided by a dissolving fluid. Now that the grub is firmly attached by both its tail and head to the tarantula, it begins to suck the juices out of the tarantula's body. As it feeds, the larva grows, rapidly engorging itself on the tarantula and darkening in color. As it grows, it molts several times, casting off its head capsule and body skin. After each molt, it resumes feeding, often through a new perforation. By the fourth instar, the tarantula's abdomen has collapsed slightly. At the fifth and last instar, the larva has developed a pair of stout, three-toothed mandibles to keep up with its feeding habits.[6] The larva has become muscular and mobile by this stage. It cuts a hole into the tarantula's carapace and thrust its head and thorax inside the host spider, continuing to feed ravenously. As it feeds, it hollows out the tarantula, up to the bases of the spider's hairy legs.[6] At the beginning of this invasive assault, the tarantula finally expires. This entire process from egg to fifth instar takes around 35 days total.

The well-nourished grub begins to spin a delicate framework to support its cocoon. The Hemipepsis cocoon is a brown, silk structure. It is slightly wider at the end from which the wasp will emerge. The inner wall is varnished, but no inner cocoon is seen.[8] Completion takes several hours, and at the end of it, the grub evacuates its alimentary canal; this meconium, or first stool, becomes a hardened mass at the end of the cocoon. The grub is much smaller than it was at the end of feeding because it has expended so much body content on spinning the cocoon and voiding its alimentary canal. The cocoon turns a greasy amber yellow from the original silky gray. The time of hatching is dependent on the season. A cocoon formed early in the summer may hatch the same summer, but a late summer or autumn brood may remain in cocoon form until the following spring or summer.[6] Once the grub reaches the pupal stage, the grub lies extended and quiet. The head capsule splits along the midline, and a glassy, whitish pupa forces its way out of the discarded, shriveling larval skin. The pupa turns creamy yellow, with gray-blue, large compound eyes showing through the thin integument. One can also see the antenna, stubby wing pads, and back spines.

A young wasp digging out of the ground

As the enclosed wasp develops, the pupa darkens. A sharp scratching noise can be heard as the young wasp cuts its way out of the tough cocoon with its strong mandibles.[6] The hatched cocoon contains the remains of the larval skin, pupal skin, and waste from the larval stage and the young wasp. The young wasp then digs its way out of the underground cell.

The breeding season of H. ustulata occurs over a two-and-a-half-month period.[9] Individual males actively seek mates on mountain ridges for up to three weeks at a time. Many males live more than one month.

How these wasps communicate with each other is unknown, especially within the aggregates they form. However, the powerful residual odors, flight patterns, and flashy colors are all likely candidates for how they communicate with each other.[6]

A palo verde tree, the territory landmark of choice of H. ustulata

Males often pick palo verde trees as landmark territories. The most preferred territories tend to be located higher up the mountain ridges.[10] During the male flight season, considerable turnover occurs in territorial ownership. The average duration of male residence is around 8 days.[10] Ownership is contested through aerial combat. Larger males have the advantage, displacing smaller males from the preferred territories over the course of the mating season. Males occur in great abundance during mating season; females are rarely seen. The operational sex ratio during this time is highly skewed towards males. In some ways, H. ustulata’s mating system resembles lek polygyny. In hilltopping insects, the male defends territories. Females may visit the territories, but they only remain long enough to mate, not to nest or feed. In a lekking species, the male-defended territory does not contain incentive of resources for females, such as food, shelter, or attractive nesting sites. Other characteristics of H. ustulata’s lekking behavior include the existence of a mating arena, where males aggregate year after year, with each male protecting its own perch/display territory and receptive females mate selectively and upon the inspection of the territorial males.

The tarantula hawk wasp returns to the same prominent plants, namely palo verde trees (Cercidium microphyllum), year after year during mating season. The preference rankings of perennial territories in one mountain ridge area remain highly consistent from generation to generation.[10] Indirect evidence shows that the stability of male preferences from year to year indicates that the access to females is related to the ability of acquiring high-ranking territories.

Oftentimes in the natural history of a species, large body size confers reproductive advantage. This raises the question in H. ustulata: Why do smaller wasps persist? Generation after generation, wide size variation exists among these tarantula hawks. Wasps do not grow after metamorphosis, so smaller animals are at a permanent disadvantage competing against their larger fellows. John Alcock's studies emphasize the importance of size variation in claiming desirable territories among male H. ustulata wasps. Female provisioning behavior may play a role in the maintenance of size variation in this species.[4] In tarantula hawks, the size of the offspring is determined by the mother's decision on how much to invest in each offspring. The size of the tarantula captured by the mother wasp determines how big the larva will become when fully grown. The subduing of a larger tarantula requires a greater energy investment and poses a greater risk to the mother wasp. If the offspring is a large male, it would have to be twice as fit as a smaller male offspring to repay the investment of the mother wasp. Thus, in some cases, it may be advantageous for the mother wasp to produce many small, male offspring. This would enable them to enjoy the same level of fitness as a female, but with fewer, larger progeny.

Territorial males of this species perch upon prominent vegetation at high elevation (1500 m or higher) and chase intruders away.[4] No more than one individual occupies each territory for more than a few minutes. Every so often, the landowning male wasp makes short, regular flights out from his perch. Intruding visitors are common among this species, as males jockey for the best territory. On occasion, the intruder engages in aerial combat with the territory owner over possession of the perch, a tree or bush. The two males clash wings and spiral vertically upwards, engaging in an aerial contest for the territory.

H. ustulata larvae feed on tarantulas that are paralyzed and captured by the adult wasps. Adult wasps spend lengthy periods of time patrolling, actively searching for prey on the ground. Adult wasps feed on nectar, and they visit flowers and flowering plants during the day. Popular sources of nectar include milkweeds (Asclepias) and western soapberry trees (Sapindus saponaria).[8]

The debilitating, painful sting of H. ustulata deters nearly all predators. No examples of amphibian, reptilian, or mammalian predation of adult tarantula hawks are known.[8] The only documented examples of tarantula hawk predation are of kingbirds in Puerto Rico, discovered by a respected entomologist, Dr. Punzo, who observed two instances of roadrunners attacking grounded tarantula hawks.[4] However, if those tarantula hawks were healthy at the time of attack, or if they were male or female, is not known. Instances of predation by roadrunners in the literature are rare at best, even on harmless males, which speaks to the defensive effectiveness and reputation of tarantula hawks in the animal kingdom.

Tarantula hawks exemplify evolutionary success in insect defense. Justin Schmidt, from personal communication with John Alcock, the world's leading H. ustulata expert: “They are aposematic, brightly colored and odored, and have hard, closely fitting, smooth and slippery integumentary sclerites, live long, form defensive warning aggregations, and even have sharp and effective defensive leg spines.”[8] Unquestionably, they are some of the best-defended insects on earth. The well-documented descriptions of battles between tarantula hawk and tarantula evidence their defensive strength. In the jaws of one of the largest and most powerful spiders on earth, the tarantula hawk still almost invariably escapes unharmed. During their violent encounters, one can often hear loud crunching or snapping sounds as the tarantula attempts to crush the wasp in its jaws. Not a single wasp death in 200 tarantula encounters was recorded by Petrunkevitch, and only one wasp injury was observed in William's extensive field studies. Their strong, slippery integumentary armor allows the wasp to slip away unharmed.

How can an essentially nontoxic venom that causes so much pain, described as blinding, debilitating, and shockingly electric by Schmidt, subside in only three minutes in humans? Only the bullet ant is ranked higher than the tarantula hawk's sting on Schmidt's sting pain index. How does it permanently paralyze a tarantula, yet keep it alive? It is also evolutionarily interesting and significant how such a toxin evolved. Selection pressure by potential vertebrate predators would have favored individuals with painful venom components, but not vertebrate-lethal components. At the same time, selection pressure against venom lethality towards prey and subsequent loss of prey to spoilage would be very strong. The tarantula hawk's venom is a specific, evolutionarily tailored cocktail of compounds best suited to the wasps’ needs. Studying tarantula hawk venom may help us gain insight into treating human problems like chronic pain from injury or disease.

An example of aposematic coloration in H. ustulata

H. ustulata and fellow members of its tribe of Pepsini tarantula hawks are well known for their aposematic coloration. They range from shiny black to blue-black with bright yellow, orange, or red wings – classic warning colors for experienced predators to stay away and keeping naïve predators wary. Tarantula hawks also emit an aposematic odor, which deters predators.[6] Such a foul odor, associated with an excruciatingly painful sting, makes a strong impression on predators, keeping them away.

All tarantula hawks derive protection from their convergent coloration. Female tarantula hawks benefit from fellow females educating potential predators to stay away with their painful stings. Male tarantula hawks, which are stingless, benefit from their resemblance to females. Other species also gain protection through both Müllerian and Batesian mimicry of tarantula hawks.[6] The strength of this mimicry speaks to the defensive power of the Hemipepsis sting.

When roaming for tarantula prey is unprofitable, these wasps form aggregations for both defensive and food-finding benefits. The presence of so many individuals reinforces the signal that each wasp sends to potential predators to stay away. Additionally, being part of a large group reduces each individual's chance of being attacked. Apart from its defensive value, such aggregations are also observed to benefit by aiding the wasps in locating nectar and by increasing mating opportunities.[6]