First human-vinegaroon encounters evoke a natural human response: “what a bizarre animal,” “is this thing real, or did someone cobble together various parts from nature? “Is it from outer space?” No, vinegaroons are real, live, arthropods, and not extraterrestrial, albeit extremely ancient. They were around during the Carboniferous era, about 350 mya, and have remained little changed “living fossils” since then. Their origin long preceded that of mammals, birds, reptiles, or modern amphibians or sharks. Vinegaroons are large, squat arachnids sporting massive pedipalp “pinchers” on the front and a tail, often longer than the body, sprouting from the other end. As if this were insufficient, vinegaroons also possess a pair of long sensory legs frequently appearing to probe randomly the environment around them. Vinegaroons are also called whipscorpions, or whiptail scorpions, monikers originating from their close phylogenetic relationship to scorpions plus their long flagellar tail that “whips” around when they are excited. Although accurate scientifically, these common names are unfortunate because they wrongly imply that these creatures can sting or are venomous. They do not have venom, cannot sting, and do not even pinch.
Vinegaroons’ true fame lies in their ability to spray a potent allo-mone which renders memorable first agonistic human encounters with vinegaroons. The whole environment instantly becomes redolent with the smell of vinegar, a result of discharge of highly concentrated acetic acid, plus a few other acids, from the pygidial glands. This cocktail contains the highest concentration of acid found in any known chemical defensive secretion, having an acetic acid concentration about 15 times that of vinegar. Is it any wonder that these animals were called vinegaroons and have become subjects of folklore throughout many areas? The acid blend is contained in a pair of glands located in the posterior of the animal and can be discharged in a well-aimed spray leaving a mobile turret where the tail joins the body.
TAXONOMY AND BIOGEOGRAPHY
Vinegaroons comprise a small arachnid (spiders, scorpions and their kin) order, the Uropygi, containing around 115 species in 16 genera. They caught the attention of Linnaeus, but were first described as a separate order by Latreille in 1802. Mainly tropical in distribution with the majority of species in Indonesia and Southeast Asia to India, uro-pygids have a smaller species concentration in the New World, especially around northeastern South America. Not surprisingly because of their antiquity that long preceded the breakup of Pangaea and their apparent resistance to extinction, vinegaroons are found on all continents except Australia. They are also found in some unexpected places including Fiji and the Solomon Islands. Most species live in moist habitats, though several, notably Mastigoproctus giganteus, the largest of the species, live in arid regions, albeit they are active only during the wet part of the summer season and days and times within the season.
BIOLOGY AND LIFE HISTORY STRATEGIES
Even experienced biologists rarely encounter vinegaroons in nature, something that leads to a general perception that these animals are rare. Vinegaroons are strictly nocturnal, with no hint of being crepuscular even to the extent of taking advantage of the last dying glimmers of light on the horizon. During 15 years and 1000 + hours in the field, I have only once observed a vinegaroon during the day-and that was just before sunset on a cloud-blanketed, rainy day. Additional factors rending vinegaroons effectively invisible are their dark, often dust covered, black color, their slow infrequent movement while active, their lack of attraction to visible or UV light, and their lack of UV fluorescence so conspicuous in their near relatives, the scorpions. When these factors are combined, is it any surprise that vinegaroons are absent in the everyday human experience?
For more than two centuries, the inapparency of vinegaroons handicapped our knowledge. Other than a few relatively recent brief descriptions of their courtship behavior and chemistry, almost nothing was known of their biology. Fundamental information addressing life span, number of eggs produced per female brood, hunting behavior and prey captured, and predators was lacking. We now know that for M. gigan-teus, the average life span from egg through completion of the adult cycle is 7 years with a potential limit of 11 years. The life cycle consists of egg; phoretic larva, four free-living larval instars, and adult. Unlike tarantulas, in which adult females continue to molt over their long adult life span, adult vinegaroons cannot molt again and both sexes generally live three summer seasons. In Arizona, each immature instar requires a minimum of one year of development before molting, with individuals having the ability to overwinter if necessary in the same instar to continue foraging a second year for sufficient prey to enable molting. This plasticity in instar length is an ideal adaptation for an animal living in an unpredictable arid environment sometimes experiencing a scarcity of available prey subsequent to little or no rainfall during the summer.
Most of their lives, Mastigoproctus giganteus reside in cells they excavate in the soil or under rocks. When the soil permits, adult cells are 30-50 cm below the surface, an environment with higher humidity and a moderate temperature during both summer and freezing winter. Vinegaroons are ambush predators, spending much of their active time in a sit-and-wait position or slowly walking and ready for any hapless small animal to come nearby. Despite their lethargic, sluggish appearance, they are acutely aware of their surrounding environment, something that becomes frustrating to humans standing several meters away and hoping to obtain a glimpse of their natural behavior. This awareness is primarily through detection of substrate vibration via an assortment of sensory sensilla, including long delicate trichobothrial hairs located at the distal end of the tibia of both sensory and walking legs. These fine trichobothrial detect even the most subtle of air movement caused by an insect moving nearby. Olfaction and detection of surface chemicals undoubtedly also play key roles in vinegaroon environmental monitoring, but detailed examination has not occurred. When an organism of suitable size comes within range, the vinegaroon springs into action with a lightning fast rush and grabs the prey. Captured animals are securely held with the pedipalps while knifelike and crushing chelicerae cut through the toughest of prey cuticle or integument.
Prey include virtually anything within an acceptable size range. Common prey include scarab and other beetles, crickets and grasshoppers, spiders, scorpions, solifugids, and even the occasional ant. Small vertebrates including newly metamorphosed spadefoot toads are also taken. One might wonder how they overcome spiders, scorpions and solifugids. The key appears to be their surprise factor and the ability of the large pedipalps to hold potentially dangerous prey distant from nonarmored sensitive body areas. Prey chemical defenses, sequestered toxins, and stings have minimal deterrence value-for example, they eat Calosoma beetles, blister beetles, honey bees, and scorpions-although some extremely well defended species including stink beetles (Eleodes spp.) and giant velvet mites (Dinothrombium sp.) are rejected.
One might imagine that a large, juicy, slow vinegaroon might have numerous predators. The opposite is the case. Over years of experimentation in which M. giganteus has been challenged by numerous and varied vertebrate and invertebrate potential predators, no examples of successful predatory species that normally encounter adults or fourth instar immatures have emerged. A reason for this paucity of meaningful predation is rooted in the exceptional deterrence of the vinegary allomone discharged by threatened individuals. Rodents, lizards, toads, spiders, centipedes, large carabid beetles, and solifugids flee and rub affected body parts in the soil when struck with the chemical discharge. Even voracious and determined grasshopper mice (Onychomys spp.) are unlikely to be serious predators because when sprayed they flee and plow their mouths through the sand, giving the vinegaroon ample time to escape. Even if the mouse is strongly hunger driven and can relocate the vinegaroon after an encounter, the vinegaroon can discharge its defense 10 or so times, each time giving it an opportunity to escape once again (Fig. 1 ) .
This a good point to digress slightly to address the commonly asked question “why does a vinegaroon have a long tail?” Defensive encounters provide the apparent answer. Vinegaroons are built much like an
FIGURE 1 Vinegaroon (Mastigoproctus giganteus) fourth instar immature (body length excluding pedipalps = 4 cm).
army tank towing food wagon behind. The front cephalothorax (pro-soma) of the vinegaroon is heavily sclerotized, armored, and nearly impenetrable. The posterior opisthosoma, however, is soft, delicate, and easily penetrated. Any predator which successfully attacks and punctures the opisthosoma will inflict a mortal wound to the vinega-roon. The mobile lashing tail gives an extra body-length margin of safety around the vulnerable posterior by detecting intruders before they can attack. Additionally, it provides an expendable decoy to be attacked first. Because the defensive spray emanates from the tip of the last three segments of the mobile turret at the end of the opisthosoma near where the tail is attached, it can be deployed instantly in a precision blast when the tail is attacked. Solifugids exemplify the system. Attacking solifugids easily outmaneuver vinegaroons, usually resulting in a posterior attack involving the tail. They become beneficiaries of a thorough spraying, immediately terminating the attack and usually preventing future attacks. In such attacks, the tail is frequently injured or lost, something that does not cause serious harm or prevent future use of defensive spray. The tail is also regenerated upon molting. The decoy value of the tail is supported by the frequency of field observation of animals’ missing part or all of their tails or sporting regenerated tails.
In good habitats, vinegaroons appear to be the most important top predators of arthropods. In a good year, in one ideal habitat of sandy-loam soil in Southeast Arizona, USA, 1748 vinegaroons were located by mark-recapture methods in a 2.56 ha plot. Their combined weight was 5420 g. These figures translate into 68,300 vinegaroons per square km for a weight of 212 kg/km2. In this habitat during the summer, is it any wonder that relatively few arthropods are observed on the soil surface, yet insects are in abundance resting on vegetation and coming to UV black lights? No other predator of medium and large arthropods is present in the system in the numbers and weight of vinegaroons.
Vinegaroons were among the first animals to help usher in the era of chemical ecology. Acetic and octanoic acids were identified by derivati-zation, crystallization, and infrared spectroscopy in an elegant chemical analysis. Nearly 40 years later, using newer microtechniques, the secretions of individuals of the four larval instars and adult males and females were reinvestigated in search of minor components and hints of subtle biological roles for the secretion. Enriching the major components of acetic and octanoic acid are trace amounts of hexanoic, heptanoic, cis-and trans-5-octenoic, and decanoic acids, plus the ketone 2-nonanone. The secretions of females, males, and all immatures are nearly identical, essentially excluding pheromonal roles (except perhaps aggregation pheromone; and vinegaroons are entirely solitary animals at all times except mating and maternal care of young). All eight analyzed other species among four genera of vinegaroons also contain a predominance of acetic acid, along with species-specific additional minor components. These findings indicate that the chemical spray is strictly defensive, and this highly effective defense has been conserved throughout the order.
COURTSHIP AND REPRODUCTIVE BEHAVIOR
The vinegaroon courtship ritual is remarkably complex. Courtship is initiated by males during the summer-active season, although females are far from placid in this process, with virgin females likely remaining active on the soil surface more than mated females. Overall, courtship lasts an average of 13 hours and goes through four phases. Phase 1, “Chase and Grapple,” occurs when a roving male contacts a female. The result sometimes appears to be a “fight to the death” in which the male rushes the female, engages her with his massive pedipalps and the two wrestle, push, and shove, often lifting one another off the ground. This is a testing period in which the female is assessing the male for fitness (female choice). But the male, too, is testing. A particularly lethargic, or old, female can be rejected by a male. The Chase and Grapple phase lasts from 1 minute to several hours, sometimes ending when the female escapes and terminates the courtship. If she is receptive, and the male is acceptable, frequently she will “present” the tips of her sensory legs to the male. She does this by rapidly quivering them in front near his cheli-cerae. If he accepts her offer, he manipulates her sensory legs with his pedipalps and transfers their tips to his chelicerae, marking the second stage of courtship. The Chase and Grapple phase can be complete in as little as 1 minute after initial contact. Many times the female is not immediately receptive and grapples, sometimes vigorously, with the male. In this situation, she holds her sensory legs far back and away from the male’s reach. Meanwhile, the male attempts to reach over her to grab her sensory legs, often near their base, with his pedipalps. If she ultimately accepts him, she will cease resisting and allow the male to hold her delicate sensory legs in his gnashing jaws. She can signal rejection by executing tiny rapid flicking of her sensory legs along with the rest of her body, often resulting in termination of courtship (Fig. 2).
Phase 2 of courtship is called “Dancing.” In this phase, the male is face-to-face with the female, and while still holding the female’s sensory legs in his chelicerae, he manipulates them with his pedi-palps and tows her forward and back. The female usually passively follows the male’s lead. The purpose of this phase which lasts 2.9 hours (range 1.25-6.25) appears to be to provide further opportunity for the male and female to evaluate each other, but it likely is also a means for the pair to move to a secure place, such as the female’s nest or a rodent burrow, to continue the courtship.
Phase 3 of courtship is energetically costly for the male and is the most consistent in duration. This phase, called ” Generation, ” starts when the male, still holding the female’s sensory legs in his chelicerae, rotates from being face-to-face with the female to being in front and on top of her with his opisthosoma elevated over her cephalothorax. The receptive female then gently holds his opisthosoma at segments 6 and 7 with her pedipalps. After a brief period of adjusting position slightly, the pair remains quiescent for 4.6 hours (range 3.5-6.0). During this phase, the male is forming a spermatophore inside his reproductive system. Near the end of the generation phase, he touches his gonopore to the substrate and deposits the spermatophore consisting of a stand holding two sperm packets. He next carefully and slowly walks forward, pulling the female to the exact spot where her gonopore is directly over his spermatophore. She then dips down and grasps the two sperm packets of the spermatophore in her gonopore, leaving the stand attached to the substrate. She now signals the male by slowly opening her pedipalps. He then slowly rotates, all the while still holding her sensory legs in his chelicerae, to face her again and advances over her top, finally releasing her sensory legs as his cheli-cerae pass over her anterior cephalothorax. Once the sensory legs are released, he often makes a quick rush to wrap his pedipalps around her opisthosoma. This release terminates the generation phase.
Phase 4 of courtship, “Pressing,” consists of the male above the female with his pedipalps wrapped around her opisthosoma and pedi-palp tips gently stroking the sperm packets for several hours (mean 4.8, range 2.0-7.0 hours). Such stroking is presumed to facilitate movement of the sperm from the packets into the female’s reproductive track. Courtship is completed when the pair separates after an unknown signal and goes their separate ways. Neither partner is injured during courtship, and post-courtship cannibalism never occurs.
FIGURE 2 Courtship ritual. Clockwise from upper left: Dancing—note female sensory legs being held in male chelicerae, Generating, Pressing, posterior view of male stroking sperm packets during Pressing phase—note empty spermatophore stand attached to ground below sperm packets.
Fecundity, Embryogenesis, and Maternal Care
At the end of the summer foraging, vinegaroons retire to overwintering cells which they seal from the surface with a soil barrier. They do not hibernate during this period of waiting until the next summer and remain alert and active if disturbed. In the spring about 2.5-3.0 months before the next summer, mated females generate an enormous clear nursery sac attached to their gonopore and fill it with large white round eggs. The number of eggs is 52.5 ±8.3 SD, range 35-68 (n = 20). Embryos develop inside the eggs within the nursery sac for about a month, then molt to white, plump phoretic larvae that leave the sac to climb onto the dorsal cephalothorax and sometimes opisthosoma of their mother. Here they attach permanently and continue developing for about another month. The phoretic larvae molt into first instar free-living larvae and crawl off their mother to distribute within the overwintering cell. At this stage, they look nearly identical to adults except their pedipalps, and appendages are pink and their sensory legs and tails are relatively longer compared to their bodies than in adults. They also have a full complement of vinegary allomone. Mother and babies remain in the cell until all young are completely sclerotized and hardened and the summer rains have arrived. The rather thin mother then digs to the surface and begins foraging. Her first instars remain in or near the maternal burrow. Although not documented in the field, mothers in the laboratory capture prey and share it with the young. This maternal care continues throughout much of the foraging season, at which time the young disperse and dig their own individual overwintering cells. Mothers do not eat their young barring exceptional hunger or situations, although they eat their own young the next year once they have molted to second instars. Mothers mate during their maternal care summer, overwinter again and can rear another set of young the next year.