Glauco Machado, Ricardo Pinto da Rocha & Gonzalo Giribet

Origin of the name Opiliones

          The name Opiliones, proposed by the Swedish zoologist Karl J. Sundevall (1833), derives from the Latin word opilio, used by the Roman dramatist Plautus (254–184 BC) in his comedies and meaning “sheep-master” — one of the various categories of Roman slaves. Virgil’s Eclogues, written in 37 BC, also mentions the word opilio, but alluding to a shepherd. This association is probably related to the elevated body position afforded by the long legs of certain harvestman species, thus resembling ancient European shepherds who used to wander about on stilts in order to better count their flocks. The earliest allusion to the order Opiliones in modern literature probably occurred in The Theater of Insects by Moffett (1634), in which they were called shepherd spiders, a name still used in Great Britain nowadays. The author explained that people called them shepherds because they thought that the fields in which they were abundant constituted good sheep pasture.

Figure 01

          The most popular common names in England nowadays are harvestmen or harvest spiders, probably because some species are quite abundant in the harvest season. Another hypothesis is that the convulsive movement made by their legs after they have become detached from the owner’s body (a common defensive behavior in some species of the order) resembles that of the harvestman’s scythe. The meaning of many common names in European countries is “reaper” (see Table 1), and this also may be related to the harvest period or to the appearance of reaping, as with a scythe, when they walk. Curiously, in some provinces of Spain harvestmen are called pedros in allusion to Saint Peter’s Day (June 29), which falls within the harvest season and is a time when some species are especially abundant in the fields. Apparently the common names used in the Netherlands and South Africa, which mean “hay wagon” (see Table 1), also allude to the harvest period.

Figure 02

           In countries where the opiliofauna is dominated by long-legged species, the common names generally make reference to this characteristic morphological trait. Good examples are daddy longlegs, used in North America and Australia, arañas patónas, used in Mexico, and suhe juzine and matija, used in Slovenia (Table 1). In tropical regions, especially in South America, where the opiliofauna is mainly composed of robust and short-legged species, the common names are usually related to the bad smell released by the scent glands located on the anterior margins of the body, a unique morphological feature of Opiliones. In Argentina they use the words chincha or chinchina, which are also applied to stink-bugs of the order Heteroptera (Table 1). In Brazil names such as bodum, aranha-bode, aranha-fedorenta, aranha-alho, and frade-fedorento are all related to the strong sour smell secreted by the large gonyleptids (Table 1), by far the most common family in the country.

Figure 03

Harvestmen in the folklore

          Biologists know little about the order Opiliones, even though it constitutes, after the Acari (mites and ticks) and Araneae (spiders), the third-largest group of arachnids. In many countries the general public largely ignores harvestmen as well. Perhaps because most species have secretive habits, live in damp and shadowed areas, are dark colored, and are active mainly at night, their existence passes almost unnoticed by humans, which may explain their virtual absence in mythology, folklore, and history. It is worth noting that Robert Hooke (1665), the inventor of the microscope, mentions in his book Micrographia an old superstition of the county of Essex, England, involving harvestmen. According to the tale, killing harvestmen on purpose would bring bad luck because supposedly these mystical animals would help the farmers harvest the crops with the scythe they were alleged to possess. On the other hand, harvestmen do not have such good fame in the United States and Australia, and there is a persistent urban legend that they are extremely poisonous, although their mouthparts are too tiny to inflict wounds on humans. Harvestmen, however, are beautiful arachnids that pose no danger to humans. There are several explanations of the origin of this legend, but the most plausible is the confusion regarding the name “daddy longlegs,” which is also used for spiders of the family Pholcidae in those countries. Since some pholcids regularly prey on other spiders — including the redback spider (Latrodectus hasselti), whose venom can be fatal to humans — it is possible that this fact has originated the rumor that they are the most dangerous spiders in the word. However, because of their tiny fangs, pholcids, like harvestmen, are completely harmless to humans.

Figure 04

Figure 05

A little bit of morphology and systematics

           In terms of general morphology, harvestmen are typical arachnids. They have two basic body regions, a prosoma, which carries all the appendages, and a limbless opisthosoma (Figure 1), which has the spiracles and the genital opening, often covered by an operculum. The junction between both body regions is not constricted, giving them the appearance of “waistless” spiders. Because of the superficial resemblance between harvestmen and their most famous cousins of the order Araneae, one of their popular designations in German is Afterspinne, that is, “false spider.” Another common German name, Weberknecht (“weaver’s helper”), is also an allusion to harvestman morphology; the second pair of legs is elongated in most species of the order and functions like an antenna, waving in the air while the animal is walking (Figure 2), thus resembling the arm movements of a weaver’s helper disentangling the threads on a loom. Another meaning is “tailor’s apprentice” because harvestmen cannot make webs. It is interesting to note that the use of the word Weber (weaver) has led to the wrong idea that harvestmen, which have no spinning organs, can produce silk.

           Harvestmen are among the oldest arachnids, and the fossil record demonstrates that the group has remained almost unchanged morphologically over a long period, a phenomenon called stasis. Unique characteristics of Opiliones, such as paired tracheae, the penis, the ovipositor, and the openings of the scent glands, are already observed in fossils from the Devonian (Figure 3), proving that the group has lived on land and that males transferred gametes directly to females as early as 400 million years ago. In fact, harvestmen are considered one of the most primitive forms of arachnid, possibly closely related to scorpions, pseudoscorpions, and solifuges; together these four arachnid orders form a clade called Dromopoda (Figure 4). However, the exact phylogenetic position of Opiliones within the class Arachnida remains a contentious issue in systematics.

Figure 06

          The first harvestman species to be described were Phalangium opilio (Figure 5a) and Trogulus tricarinatus (Figure 5b), named by Linnaeus in 1758. Since that time some 6,000 species have been described by more than 110 taxonomists, of whom half described more than 10 species. Nearly 200 harvestman species scattered around the world were described between the 1870s and the first decade of the twentieth century (Figure 6), when Eugène Simon, Tord Tamerlan Theodor Thorell, William Sørensen (Figure 7a), and Nathan Banks, among others, introduced more than 700 new species. An intense descriptive period occurred between the 1910s and the 1950s, when the German author Carl Friedrich Roewer (Figure 7b) was most active, describing more than one-third of the species in the order Opiliones. He created a new system of classification, and his book Die Weberknechte der Erde, published in 1923, is a landmark, containing the 2,000 harvestman species known until that time and many descriptions of new taxa. Roewer’s age was also a time of other important prolific taxonomists, such as the Brazilian Cândido Firmino de Mello-Leitão (Figure 7c) and the South African Reginald Frederick Lawrence (Figure 7d). Some years later, between 1940 and 1980, the American couple Marie Louise and Clarence Goodnight (Figure 7e), the Brazilian Hélia Eller Monteiro Soares (Figure 7f), and the Japanese Seisho Suzuki (Figure 7g) were also very productive, describing in all almost 700 species. Nowadays, modern authors are more concerned with reviewing groups than with describing an extensive amount of taxa. Exceptions to this pattern are Jochen Martens (Figure 7h) and Manuel González-Sponga (Figure 7i), who have been working with the rich faunas of the Himalayas and Venezuela, respectively. The tropical faunas of Africa, Asia, and Central South America probably contain a large unknown diversity yet to be described, mainly in the most diverse families Sclerosomatidae, Gonyleptidae, and Cosmetidae. Minute forms, such as the zalmoxids and Cyphophthalmi, may also provide many new species, so the real richness of the order may exceed 10,000 species.

Figure 07

          Harvestmen are divided into four suborders (Figure 8) that contain 45 recognized families and about 1,500 genera. However, the limits and relationships of most families and genera are imprecise, and new families are expected to be discovered. Representatives of Cyphophthalmi, the oldest suborder, which includes six families and 130 species, are distributed worldwide, inhabiting all continents and islands of continental origin. They are among the smallest and most obscure Opiliones, typically measuring between 1 and 3 mm in body length (Figure 9a). The suborder Eupnoi includes six families and 1,780 species, and some species of this group are among the best known Opiliones. They are widely distributed in both hemispheres, and the great majority of the species are soft bodied and long legged (Figure 9b). The members of Dyspnoi (Figure 9c) present a great diversity of sizes and morphologies, including the largest harvestman species, Trogulus torosus, with a body 22 mm long. This suborder is divided into seven families containing 290 species, which are mainly found in the Northern Hemisphere. Laniatores is the most diverse suborder, composed of 26 families and 3,748 species distributed mainly in tropical and temperate regions of the Southern Hemisphere. Many representatives can reach large sizes, such as the gonyleptid Mitobates triangulus (leg IV can reach 185 mm), and some of them are colorful and/or well armed with spines (Figure 9d).

Figure 08

Where do they live?

           At the ordinal level, harvestmen are ubiquitous and can be found in all continents except Antarctica, from the equator up to high latitudes. We can find them in a great variety of habitats in all terrestrial ecosystems, including in soil, moss, and leaf litter, under rocks, stones, and debris, on vertical surfaces from tree trunks to stone walls, among grassy clumps, and running over high vegetation. The most diverse harvestman communities, however, are reported for tropical areas, especially rain forests (Figure 10). Although some species are widely distributed and can be found in a wide range of habitats, many harvestman species are much more limited in geographic distribution and habitat use, especially in tropical areas. Some species are restricted to caves, and others occur in very specific microhabitats, such as nests of leaf-cutter ants. The influence of physical factors on the spatial distribution of harvestmen has been poorly studied, but temperature and humidity seem to be the most important determinants of their distribution and habitat use. Despite this internal homeostasis, there is strong evidence that many harvestman species are inefficient in avoiding water loss. Some morphological and physiological features of the order, such as a large surface/volume ratio, lack of spiracular control, and low osmotic hemolymph concentration, may partially explain why most species are found in damp and shaded areas.

Figure 09

What do they eat?

          Most harvestman species have an omnivorous diet that includes small, soft-skinned arthropods and other invertebrates, as well as carrion, plants, and fungi (Figure 11). This broad alimentary spectrum may be considered a unique feature among arachnids, which are generally viewed as exclusive predators of invertebrates (mainly arthropods) and small vertebrates. There are a few species that specialize almost exclusively in terrestrial snails and slugs and thus have the common name Schneckenkanker, which means “snail harvestman” in German. In order to find food, most harvestman species seem to rely on an ambush strategy or, more rarely, on active hunting. Periods of waiting are generally intercalated with periods of slow movement in which the individuals, which are unable to form images and probably can only distinguish light from dark, explore their environment using the tips of their second pair of sensorial legs (Figure 2). This particular feature of harvestman biology inspired their popular name in Japan, zatomushi; zato is an ancient word used to designate the players of the biwa, a traditional Japanese stringed instrument that was generally played by blind people, and mushi means “bug.” Therefore, the name associates the walking behavior of harvestmen, with their long second pair of legs stretching ahead like arms, with a blind person fumbling along his way with a walking stick.

Figure 10

Who are their enemies?

           Unlike most arachnids, harvestmen do not have a pumping stomach to suck the liquefied tissues of their prey, and they masticate their food by ingesting small particles. Therefore, they are exposed to parasites and pathogens that otherwise would be filtered out by the feeding mechanism, as occurs in the other arachnids. Gregarines are particularly abundant in harvestmen but are uncommon in other arachnids, such as spiders. Additionally, the omnivorous feeding habits of many harvestmen place them in close proximity to contaminated materials, which may result in contact with pathogens or infective stages of some parasites. These are not the only natural enemies of harvestmen; a compilation of the literature clearly shows that the most diverse group of harvestman predators is that of passerine birds. Frogs and toads, insectivorous mammals, and spiders are other important groups of predators (Figure 12).

Figure 11

Figure 12

How do they get protection?

          To deal with this diversified range of natural enemies, harvestmen have developed a great variety of defensive strategies. Some species, for instance, camouflage themselves with debris glued on by a secretion from the integument, and very frequently they respond to predator attacks by feigning death (Figure 13), a defensive behavior known as thanatosis (after the Greek god of death, Thanatos). If disturbed, many long-legged species rapidly vibrate the body, a defensive behavior known as “bobbing” that probably confuses the identification and exact location of the harvestman’s body. Because of this last defense mechanism, in some places of southeastern Brazil the long-legged harvestman species are called aranhas-bailarinas, and in Costa Rica they are known as pendejos (Table 1).

          As we have seen earlier, many common names attributed to harvestmen around the world are related to the bad smell of their scent glands and to their leg movements after they are shed. These two defensive strategies are so conspicuous that they have even attracted the attention of non-experts in the group, such as the famous Spanish painter Salvador Dalí, whose interest in bizarre animals is quite evident in his works. In his 1940 painting Daddy Longlegs of the Evening — Hope! Dalí carefully illustrated two common defense strategies in Opiliones (Figure 14). The harvestman, clearly a representative of the suborder Eupnoi, occupies a central position in the painting and has lost one of its legs, a defensive strategy known as autospasy. Moreover, the individual is surrounded by a swarm of ants that fail to contact the harvestman’s legs, probably because of the action of scent gland secretions, which are known to be a highly effective repellent against these insects. Although the atmosphere of the painting is bleak, the harvestman is a reference to an old French peasant legend that says that the sighting of a harvestman in the evening hours is a good omen, a portent of good luck, and a symbol of hope. Interestingly, the harvestman’s common name in Turkish (müjdeci or mücdeci) suggests a similar symbolism, since it means a person who brings good news (Table 1).

          Unlike other arachnid groups, many species of Opiliones seem to be highly tolerant of conspecifics. Several species form dense diurnal aggregations consisting mainly of subadults and adults of both sexes. In general, individuals aggregate at protected sites and close to a water source. The number of individuals in these groups ranges from 3 to nearly 200 among the Laniatores (Figure 15), but among the Eupnoi there are records of mass aggregations containing more than 70,000 individuals. One of their common names in the United States, “grandfather-graybeard,” is probably related to these huge aggregations since individuals are facing upward and their long legs are hanging down, resembling a beard or wig. Although gregariousness in harvestmen seems to be primarily induced by environmental factors, this behavior may confer several defensive advantages, including strengthening of defensive signals through the collective release of scent-gland secretions, speeding the response to alarm signals provided by the scent secretion, and decreasing each individual’s chances of being eaten (dilution effect).

Figure 13

Harvestmen reproduction

          The great majority of harvestmen reproduce sexually, although some species reproduce asexually by parthenogenesis, and the sex chromosomes have been identified as usually XY-XX. As we saw earlier, harvestmen may have been the first group of arthropods to evolve an intromittent organ, this being another unique morphological feature of the order among arachnids (Figure 16). However, the study of mating strategies is probably the aspect of their behavior that has received the least attention. Harvestman fertilization is internal, and the transfer of spermatozoa may occur indirectly through spermatophores (in Cyphophthalmi) or directly by means of long and fully intromittent male genitalia in the other suborders. Unlike courtship in other arachnids — a process in which males must first “persuade” the female not to consider them as prey and that may require a careful approach and a long-distance, elaborated, highly stereotyped, and species-specific visual or vibratory set of displays — courtship before intromission is often quick and tactile in harvestmen. In some cases, however, males may offer a glandular secretion of their chelicerae before copulation as a nuptial gift for their mates. Many studies also mention intense courtship during intromission and mate guarding after copulation. Additionally, males of many species defend territories, which are used by females as oviposition sites. Given the amazing complexity of the male genitalia and the enormous diversity of types of sexual dimorphism, sexual selection (be it intra or intersexual) has probably played a major role in the evolution of harvestmen.

Figure 14

Figure 15

Figure 16

Figure 17

Figure 18

          Females may lay their eggs immediately or months after copulation, and the eggs may take from 20 days to more than five months to hatch. The forms of parental care may include the production of large yolky eggs, the preparation of nests, the choice of appropriate oviposition sites, and parental care (Figure 17). Although maternal care is widespread among arachnids, harvestmen are the only order in which some species present exclusive paternal care, the rarest form of parental investment among arthropods. Both maternal and paternal care have been demonstrated to play a crucial role in egg survival, preventing predation and fungi attack. However, the selective forces leading to the evolution of these two forms of parental assistance seem to be very different. Since the great majority of maternal harvestmen are restricted to a single reproductive event during the breeding season, females can achieve greater reproductive success by remaining close to their hatchlings throughout the caring period. Thus maternal care is likely to have evolved as a result of natural selection. In contrast, male care in harvestmen seems to have evolved as a result of sexual selection. According to recent studies, males that provide paternal care are preferred by females and obtain a greater number of copulations than males that are unable and/or unwilling to provide care.

Threatened species

           Although harvestmen are a fascinating group of arachnids, the dramatic increase in environmental disturbance around the world — especially in tropical regions — may have driven many species to extinction even before their formal description by taxonomists. Many human activities, including pesticide use, forestry operations, air and soil pollution, fire, and even the introduction of domestic animals, have tremendous impacts on the habitats on which harvestmen are dependent. Most harvestman species have restricted distributions and can be particularly endangered if human activities unfavorably alter their habitats. This is the case for most cave dwellers, which may be driven to local or complete extinction if the cavernicolous habitat or the nearby external environment is severely disturbed. In fact, almost all harvestman species formally considered endangered around the world are cave dwellers, although many other species living in other habitats may be equally endangered. However, given the paucity of ecological information for the great majority of harvestman species, it is almost impossible to reliably report on their conservation status. Therefore, the preservation of habitats instead of particular species may be the most effective means to protect the diversity of Opiliones around the world.

Concluding remarks

           Given their geographic distribution and species richness, it is surprising that harvestmen have remained largely ignored by the general public and zoologists as well. Their behavior and ecology are just beginning to be understood, and in the last two decades the number of studies published on these subjects has increased considerably, especially in South America (Figure 18). Populations of many species are locally abundant, and individuals are easy to observe. Additionally, there are standard methods and techniques used to study harvestman biology both in the field and in the laboratory. Finally, representatives of the order may be easily maintained in captivity, where they behave in a similar way to that observed in the field. Thus, harvestmen are perfect subjects for ecological, behavioral, and evolutionary studies, and we truly expect you — whether an amateur or a professional — to join us helping progressing in the understanding of the fascinating biology of harvestmen.