Lachryphagy


Lachryphagy is the practice of feeding on tears and other eye secretions. Certain bees, butterflies, and flies have been observed feeding on the tears of reptiles, birds, and mammals, including humans. Lachryphagous insects gather nutrients, especially sodium and proteins, from the tears. Lachryphagous feeding can be unbothersome or painful, with some feeding insects damaging the eye and introducing pathogens to the host. Lachryphagy has been studied as a form of parasitism, commensalism, and puddling.
It is best known as a behavior of butterflies and moths. Flies, stingless bees, and other insects such as cockroaches and lice have also been recorded feeding on tears, and there is evidence that some stingless bee colonies in Southeast Asia have specialized tear collectors as a division of labor.

Lepidopterans

Lachryphagy is best known as a behavior of adult butterflies and moths. Tear-drinking and eye-frequenting behavior has been observed in butterflies and moths throughout tropical and subtropical regions of Africa and Asia, particularly in their "savanna belts and monsoon regions... where the dry season covers a period of at least three to four months, and where rainfall and humidity are too low for rainforests." Bänziger numbered the known lachryphagous moths in 2009 at around 100 species across six families, with 23 imbibing from human eyes. Wilhelm Büttiker and J. D. Bezuidenhout recorded the first accounts of lepidopteran lachryphagy in southwest Africa in 1974, of three species in the genus Arcyophora. They found these eye-frequenting moths drinking from the eyes of domestic cows and goats. It is also documented in South and Central American moth species, and a single account of moth lachryphagy in the United States was recorded in 1972.
Lachryphagy in lepidopterans is thought to have evolved from mud-puddling behavior, in contrast to hematophagous Lepidoptera whose behavior is thought to derive from fruit-piercing feeding. Most moths observed drinking tears are male, suggesting that male lachryphagous moths collect sodium to transfer to females during mating. Tears form the largest part of the diets of most eye-frequenting moths. Only two species, Lobocraspis griseifusa and Arcyophora sylvatica, are known to be eulachryphagous. L. griseifusa secrete gut proteases which allow them to digest proteins in tears, making it the only lepidopteran adult capable of digesting proteins. Lachryphagous behavior among moths seems to be limited to nocturnal species, likely because hosts are less alert at night. It has been proposed that lachryphagous moths drink tears due to a scarcity of flowers or in pursuit of essential salts.

Hosts

The wild and domesticated mammalian hosts of moths include antelope, elephants, horses, mules, pigs, sambar deer, sheep, tapirs, water buffalo, and cattle. Butterflies have been observed drinking the tears of reptiles, including turtles and crocodiles. Lachryphagic moths generally do not specialize in any host species, and generally prefer large hosts, who are less reactive and sensitive to the moths. Lachryphagy on large hosts is generally observed during the day, while lachryphagy on small hosts is more commonly practiced at night.

Birds

Moth lachryphagy on avian hosts has been documented only three times.
The first report of moths feeding on the tears of birds was published in 2007. The Malagasy moth Hemiceratoides hieroglyphica was found to probe its sharp proboscis into the closed eyes of sleeping birds at night to drink their tears. H. hieroglyphica's proboscis is unique among those of lachryphagous moths, being armored with "hooks, barbs, and spines" and "shaped like an ancient harpoon". The proboscis is similar in anatomy to those of fruit-eating and blood-sucking calpine moths, to which H. hieroglyphica is more closely related than it is to other lachryphagous moths. The researchers who observed it noted that H. hieroglyphica does not use its harpoon-like proboscis to pierce the bird's eyelid; they theorize that its barbs are used to secure the proboscis in place between the bird's eyelids while the moth feeds. This species is specialized to drinking the tears of birds because of the lack of large mammals in Madagascar, whose most common large-eyed mammals, such as lemurs, are nocturnal. David Plotkin considers it likely that H. hieroglyphica is the "most competent vector for a disease agent" among lachryphagous moths.
Two cases have been observed in South America: an Azeta melanea drinking from a ringed kingfisher in Colombia, and a Gorgone macarea drinking from a black-chinned antbird along the banks of the Solimões River in the central Amazon, Brazil. The antbirds appeared unbothered as they were exploited by the moths, whose large proboscises allowed them to rest on their hosts' necks. The observing researcher theorized that the birds' immobility may be explained by their lowered nocturnal metabolic rate.

Humans

Lachryphagy of human tears by moths was first observed in 1966. According to Bänziger's 1972 study of lachryphagous moths in Southeast Asia, the people most exposed to tear-feeding moths are outdoor-sleeping herders, woodcutters, porters, and caravan travelers who walk forest paths during the monsoon season to transport goods such as betel nuts, opium, and cattle. No moth is known to specialize in human tears. Experiments by Bänziger along with his observation that most incidents of human tear-feeding occurred when subjects were within 10 meters of a larger animal host suggest that humans are not attractive hosts—"certainly less so than water buffalo".
According to Bänziger, Thai villagers are often reluctant to associate eye diseases with moth lachryphagy "due to their respect for nature and fear of cosmic punishment." Many locals believe that illnesses of this kind are caused by forest spirits or are punishment for trespassing into sacred areas of jungle, and are hesitant in discussing their interactions with insects. They refrain from catching or harming lachryphagous moths, and do not try to swat them away even if they land on them, instead "suffer the irritation in silence unless the annoyance becomes unbearable."

Feeding position and conditions

Lachryphagous moths drink tears directly from the eye as well as from tear-stained cheeks. Most moths circle the head before landing quickly on the face, probing for any wetness before settling at the eye. By contrast, L. griseifusa flies directly to the eye, extending its proboscis to drink after "quivering for a few seconds" upon landing. Both L. griefusa and A. sylvatica—the two known moths whose entire diet consists of tears—drink only directly from the eye, never from the cheek. Crambids like Filodes fluvidorsalis rest with their wings open, and feed from afar with the proboscis extended, while lachryphagous Geometridae, whose wings are elevated and folded at rest, feed very close to the eye. The very large hawkmoth Rhagastis olivacea, whose spiny legs would likely cause discomfort to a host, hovers in the air with its proboscis extended to drink from a human eye "with minimal interference". Bänziger described the experience as painless and less irritating than other species, like a "cool, smooth foreign body moving between the lower lid and the cornea." This suggests a correlation between morphology and feeding position in lachryphagous moths, as more obtrusively-shaped moths must avoid causing irritation to the host in order to continue their drinking in peace.
Groups of moths are commonly seen drinking together, and as many as 13 moths have been observed feeding on a single banteng's eye. Feeding groups are often mixed-species, and individual moths do not competitively drive each other away. Newcoming moths attempting to join groups of 8–10 may struggle to land and be driven away by the wingbeats of already-feeding moths as they attempt to wedge themselves into the group. Individual animals with heavy tear flow attract more moths. Bänziger and his team noted that "certain persons were visited relatively often, while others never were." Lachryphagous moths excrete excess water during and after tear-feeding.
Hans Bänziger's study of eye-frequenting moths in Northern Thailand describes mechanical damage to the eye caused by the moths' proboscises. In a later study, Bänziger described Chaeopsestis ludovicae scratching the conjunctiva with its sharp tarsal claws, causing a sensation like "a grain of sand being rubbed between eye and lid" even as its proboscis produced no irritation. Bänziger describes the sensation of Pionea aureolalis's proboscis probing his eyeball as uncomfortable, inducing a flow of tears, but not painful. Though Bänziger proposed that the probing around the eye was a deliberate maneuver to induce lachrymal flow, David Plotkin notes that this hypothesis is untested, and the probing behavior may simply be a search for an optimal feeding site. Other moths, however, elicited "stinging pain". After 30 minutes of allowing a Lobocraspis griseifusa'' to drink from his closed eye, Bänziger was so irritated that he had to stop, and for the rest of the day his eye was red and inflamed and hard to keep open. Plotkin suggested that the difference in sensation of being fed on with one's eye open and closed may be caused by contact between the host's eyelid and triangular spines on the proboscis. Plotkin suggests that this may be strategic, so as to induce the host to keep its eye open, increasing available eye surface for drinking to allow for multiple moths to imbibe. Rain generally reduces tear-feeding activity, though a brief increase is often seen at the start of a light shower. Wind strongly inhibits feeding, while temperature has little effect—moths are active in both cool and warm conditions. Activity typically rises after long dry periods or dry days following rain. Smoky fires lit by Thai farmers to keep biting insects from cattle were found to repel lachryphagous moths. Some lachryphagous moths also seemed to avoid bright lights, rarely landing on eyes illuminated by researchers' flashlights.