William A Shear. American Scientist. Volume 97, Issue 6. Nov/Dec 2009.

When I travel about the country giving talks to other scientists or to school groups about arachnids, a group of animals that has fascinated me for decades, one of the first questions to be asked after my presentation is often this one: “Is it true that daddylong-legs have the most potent venom of any animal?” Before I give you my answer, let me provide some background. The questioner is referring to an arachnid that is generally familiar to anyone who regularly visits North American forests or suburban gardens. The daddylong-legs of legend has a compact, small body outfitted with eight ridiculously long, almost threadlike legs, on which it bounces rapidly along a woodland path, or clambers in vegetation. In Europe and some parts of North America, locals call them harvestmen because they appear in fields around harvest time, and their gangling gait resembles that of a longlegged harvester swinging a scythe (in France they’re called faucheurs, literally “reapers”). Local names in other countries reflect this seasonal appearance, the long-leggedness of some species, or their resemblance to spiders. A point to be made here is that vernacular names are usually not transferable; that’s the idea of having codified Latin names for animals and plants. Using a classical language no longer spoken by anyone, and hence unchanging, allows scientists in all countries to communicate unambiguously. The Latin name of the order of arachnids that includes the daddy-long-legs or harvestmen is Opiliones, Latin for “shepherd,” which might refer to the ancient use of stilts by shepherds to get a better view of their widespread flocks.

In much of the world, the local fauna of Opiliones is dominated by very long-legged species—hence the vernacular names. But to the biologist who has made a study of these wonderful creatures, the long-legged species represent only a part of the whole. The order Opiliones also includes tiny, compact, short-legged species that inhabit the world of leaf litter and humus, as well as large, often colorful tropical species with bodies covered in outrageous knobs and spines. Numerous species dwell in deep caves and lack both eyes and pigmentation. Others disguise themselves as lumps of dirt, with special adaptations to accumulate bits of soil. As arthropods, harvestmen (my personal choice of a vernacular name) have a tough cuticle—an outer, secreted layer that serves not only as armor and waterproofing, but also as an external skeleton to which muscles attach. And like other arthropods, their legs consist of jointed, tubular sections. They are classified as arachnids because they lack antennae, carrying in their place a pair of pincer-like jaws called chelicerae. The chelicerae are followed by a pair of short appendages dubbed pedipalps, and then by four pairs of walking legs, the second, and usually longest, pair of which often function as antennae, waved about to get tactile (and probably chemical) information from the environment. The body of a harvestman is quite compact, without the two-part division that characterizes the related spiders, and unlike spiders, harvestmen can’t spin silk. A single pair of eyes often occupies a small turret hear the front of the body, but the eyes are small in nearly all forms and probably have little to do with detecting either food or enemies; like other arachnids, harvestmen live in a world dominated by the senses of touch and taste.

And what about those long legs? Is there an advantage to having legs up to 20 times longer than your body? Many functional explanations have been proposed. One involves a physical model called SLIP (spring-loaded inverted-pendulum); in this model the bouncing of the body suspended from the long legs is converted into potential energy stored in the elastic cuticle and then converted into forward momentum, providing fast and efficient running. Others have speculated that the long legs give harvestmen a very small “footprint” and keep the body off the ground where it is less likely to be directly attacked by predators such as ants. Tropical biologists have observed that some long-legged species in South America hang inverted from vegetation.with their legs widely spread—are they simulating the radial structure of a spider’s web to capture flying prey? It has also been noticed that the ends of the long legs are prehensile, curling around twigs. Maybe the long legs are adaptations to clambering about in tangled vegetation. Clearly more observations and experiments are needed before we can understand why daddy-long-legs have long legs.

More than 6,000 species of harvestmen have been named so far, but the rate of discovery of new species, especially in the American and southeast Asian tropics, is so high that we estimate this number represents less than half the total of existing forms, perhaps far less. Harvestmen occupy many habitats, from rainforests to deserts and tundra, but seem most common and diverse in forested regions. With so many species still unknown, or known only from brief original descriptions, it is no surprise that we still have a great deal to learn about these animals. But what we already know is remarkable and fascinating.

Like most arachnids, harvestmen seem to make their living as predators. They have been observed feeding on soft-bodied insects and spiders, including small (but important) plant pests like aphids and mealybugs, scavenging almost any kind of dead animal from vertebrates to earthworms, and even from time to time sucking up plant juices or picking at decaying fruit. They are the only order of arachnids in which bits of solid food are swallowed; almost all the others (like spiders and scorpions) feed only on liquids and must digest their prey externally by regurgitating enzymes, then sucking up the resulting soup. A few cases of remarkable specialization are known. At least two European species, Ischyropsalis hellwigii and Trogulus tricarinatus, are specialists on snails, but use two strikingly different strategies to attack them. Ischyropsalis have huge, powerful chelicerae as long or longer than the whole body of the arachnid, and they use these fearsome appendages to break off pieces of snail shell until the succulent morsels inside are exposed. But Trogulus is more insidious, actually pushing its way into the shell (it has a short-legged, elongated body well adapted to the task) and eating the occupant. Trogulus uses the snail to further advantage as well: females lay eggs in the undamaged shells. There may be other snail-eating strategies, or at least species that might attack heavily armored prey. Quite a few tropical harvestmen have gigantic, muscular chelicerae that, instead of being fitted out with the usual conical teeth, have heavy knobs and nodules. By analogy with large lobsters, such appendages could be used to crush the shells or exoskeletons of prey. One large group of harvestmen, the Dyspnoi, have pedipalps covered in sticky, glandular hairs. While there are few direct observations to support it, some speculate that these appendages act like flypaper, happing small arthropods until they can be raked off by special cheliceral combs and eaten. For species that capture active prey, the pedipalps are most often the weapon of choice, and many species with large, raptorial palps have arrays of interlocking spines that could act not only to hold prey, but also to pierce their bodies. One South American family, the stygnids, have elongate pedipalps with a spiky “hand” at the tip, which they can use to grab prey items at a distance.

Predators they may be, but harvestmen are themselves prey for larger animals, and may form an important part of the diets of amphibians, reptiles and birds, among other groups. But they may not be easy meals. Hard-bodied tropical harvestmen often have bodies and legs that feature needle-sharp spikes; these could make them an unpleasant mouthful. At least one tropical gonyleptid has greatly enlarged fourth legs armed with stout spines and can give even a human captor a nasty pinch. The familiar North American long-legged species, most of them belonging to the genus Leiobunum, can quickly drop off a leg or two if attacked, an ability called autospasy. The leg keeps twitching, distracting the predator. The legs themselves even have their own breathing pores to supply oxygen needed for the twitching muscles. Unfortunately for the harvestman, it appears that these self-amputated legs cannot be regenerated, and losing too many could be fatal. But I’ve seen a few specimens managing quite well with as few as three legs left—so long as there’s one on one side of the body and two on the other! It may be better not to be caught at all, so harvestmen living in the litter of the forest sometimes have cuticular structures that accumulate dirt and bits of humus. These may be short, curved setae, glandular bumps that secrete a glue, or in the case of the California genus Ortholasma, a curious grid-work, made from three-armed tubercles, that is suspended on struts above the body (as in the animal on the cover of this magazine). When coupled with the tendency of these species to play dead if disturbed, this is an effective strategy for not getting seen by a bird or toad. It also makes it difficult for biologists to collect them, perhaps explaining why so many new species are being described in this group, a particular interest of mine.

However, the most interesting defense mechanism of harvestmen is chemical. From a pair of pores (called ozopores) near the front of the body, many harvestmen can produce an array of noxious chemicals synthesized in internal glands. The exact chemistry seems to vary from group to group. For example, Leiobunum and its relatives use long-chain alcohols and aldehydes, giving them an aroma that to me smells like very old, very dirty gym socks. Corrosive benzoquinones are used by the mostly tropical gonyleptids and related families. The tiny, mite-like cyphophthalmids (about which more later) mix quiñones and alcohols. Most interesting are the travunioids, a small group of armored soil dwellers from North America, Europe and Japan. The few species that have been studied produce substances analogous to pseudephedrine (the active ingrethent of many nasal decongestants, such as Sudafed) as well as nicotine and related poisonous alkaloids. Just as the molecules vary, so does the method of application. Some harvestmen create a cloud of volatile repellent around themselves, as the fluid from the glands quickly spreads over the body and evaporates. Others can actually squirt the secretion as a jet or a fine mist. The little cyphophthalmids pick up the secretion on the tips of their legs and dab it on attackers. The Dyspnoi, mentioned above with their “flypaper” pedipalps, remain somewhat mysterious in this regard. They have ozopores and glands, but the several species that have been studied so far by myself and my chemist colleague, Tappey Jones at the Virginia Military Institute, seem to have no volatile chemical defense. It may be that their defensive system has been co-opted for another purpose, such as intraspecific communication.

Much also remains to be learned about the sex lives of harvestmen. Only a few species have been studied in detail. Sexual dimorphism, with males larger and more heavily armed than females, suggests that fights, real or ritual, may occur between males. In a few species, males may compete not just for females, but for resources. The South American gonyleptid Zygopachylus is unusual in that the males make fortress-like nests of mud in which several females may be induced to lay eggs, and males often fight over the nests. Courtship seems usually to be brief, involving a lot of leg-tapping of the partner, but in the Eyspnoi, males may offer the females a gift of an attractive secretion from glands on their chelicerae. Males have long, extensible peruses that they insert, usually in a “face-to-face” position, into the female’s genital tract. The sperm are immobile and are stored by the female until she is ready to lay eggs, which she does by means of a long ovipositor that can reach down into crevices in rocks and between soil grains. In many species, the eggs are hidden in this manner and receive no further care, but other species’ females may guard not only the eggs but the freshly hatched young. Zygopachylus is unusual, but not unique, in that the task of egg-guarding falls to the males in their mud forts. Finally, it would appear that a handful of species have dispensed with males entirely. In these species, females produce young from unfertilized eggs, a process called parthenogenesis.

Sexual relations aside, some harvestmen seem quite sociable. Several North American species of Leiobunum have been observed massing together in large numbers, usually in places like caves or culverts. These aggregations occur most frequently in cold weather, as the individual harvestmen seek sheltered spots to spend the winter. The aggregation might be just an accidental effect of all of them winding up in the same place, or it may have a defensive function. Certainly the massed chemical defense of hundreds of Leiobunum would be far more powerful than that of only a few. Aggregations that I have witnessed seem also to coordinate behavior in a way that would put off predators—disturb a cluster and they all start bouncing on their long legs, creating a pulsating mass in which it would be difficult for any predator to pick out an individual to attack. The effect is quite unsettling to the human observer.

That Opiliones is an ancient group has been demonstrated by the recent discovery of harvestman fossils in Scotland’s Devonian Rhynie Chert, about 400 million years old. The find (Eophalangium sheari), described in detail by Jason Dunlop at Humboldt University, Berlin, and colleagues, is very similar to species still living in the Rhynie region today. The preservation is so detailed that even the characteristic penis and ovipositor are preserved. A scattering of harvestman fossils are known from the Carboniferous Period, and quite a few have been found in amber deposits ranging up to 35 million years old. All of these fossils suggest there has been little innovation in harvestman anatomy for 400 million years.

Harvestmen are coming into their own as tools for the study of genetics, evolution and biogeography, all three of which are now developing into mutually supportive fields. In Japan, studies of Jjríobunum chromosomes by Nobuo Tsurusaki of Tottori University have revealed that some species have the greatest range of differing chromosome numbers of nearly any animal, and some populations may be tetraploid (with four sets of chromosomes instead of the usual two, a condition rare in animals) or have extensive supernumerary chromosomes of uncertain function. One study in which genetics and biogeography have come together has established that a tiny, bright yellow Appalachian harvestman I discovered and named in 1977, Fumontana deprehendor, is not just one species but perhaps as many as five, separated by riverine and lowland barriers. Steven Thomas and Marshal Hedin of San Diego State University found that the isolated populations are genetically distinct, but so far they have proved impossible to differentiate by their anatomy. In another case, I studied harvestmen of the genus Caddo, and found a new species in New England, Caddo pepperella, which co-occurred with another, Caddo agilis, and looked exactly like Caddo agilis juveniles—but the pepperella specimens were sexually mature. I proposed that pepperella had originated from agilis by neoteny, a developmental process in which sexual maturity is reached earlier in life than usual. This process “instantly” created a new species because both agilis and pepperella are parthenogenetic, consisting of only females. Later, both species were found in Japan. My hypothesis was that agilis had once been distributed across the northern hemisphere (fossils that look just like agilis are found in European amber, 35 million years old) and that “pepperella” had originated by neoteny twice, once in Japan and once in North America, after the extinction of intervening agilis populations. At that time it was not possible to definitively test the hypothesis of the dual origin of pepperella, but recent studies of DNA sequences in the two species by Jeff Shultz and Jerome Regier at the University of Maryland have shown that the Japanese populations of pepperella are the closest relatives of the North American populations, not of Japanese agilis, as would be expected under the dual-origin model. So my hypothesis was falsified—pepperella must have originated before the Japanese and North American populations became separated.

The cyphophthalmids, tiny, mite-like, and with small species ranges, have proved ideal for more sweeping work on the evolutionary effect of vicariance (geographical separation of groups of organisms) by continental drift. Gonzalo Giribet of Harvard University and Sarah Boyer of Macalester College have found that the phylogenetic tree of cyphophthalmids corresponds very closely to what would be expected given geologists’ reconstruction of the breakup of the supercontinent Pangea, with the deeper branches of the tree corresponding to the earliest events of the supercontinent’s fragmentation.

Now to the venom question. Do harvestmen have the most potent venom of any animal? Unfortunately for opilionologists, this chilling observation, which could spur lots of research on harvestmen, is entirely false. Harvestmen have no venom glands whatsoever, and therefore no venom, potent or otherwise. How did the story of their poisonousness get started? Probably through a misunderstanding of vernacular names. A short paper on an Australian spider asserted that “daddy-long-legs” had unusually potent venom, but in Australia, this name is usually applied to a spider, not a harvestman. When the story was picked up by American supermarket tabloids, the Latin names were ignored, and the potent venom was attributed to Opiliones.