INTRODUCTION

Lepidoptera is one of the largest insect orders, containing over 150,000 known species and found in nearly every area inhabited by people (Beccaloni et al. 2003, van Nieukerken et al. 2011). Even though lepidopterans are ubiquitous, only a very small percentage of species, as adults, have any direct medical relevance to humans. Many of these species are medically relevant because they consume human bodily fluids – specifically blood, sweat, and tears. Blood‐feeding (hematophagous) lepidopterans, also known as vampire moths, use their barbed proboscises to pierce mammalian skin and directly suck up blood (Zaspel 2007, 2011, 2012). Tear‐feeding (lachryphagous) lepidopterans imbibe lachrymal fluid, usually by placing their proboscis directly on the eye of their host (Bänziger 1992, Büttiker 1997), and sweat‐feeding (we use the term “sudophagous”) lepidopterans use their proboscis to lap up sweat from many different surfaces, including human skin (Collenette 1934). The morphology, behavior, and medical importance of these three groups of Lepidoptera are addressed in this review.

Lepidopterans that feed on humans do not use the body fluids as their lone food source; however, these fluids provide them with a crucial nutrient – sodium. Lepidoptera larvae are usually herbivorous, which generally does not provide them with sufficient amounts of salt (Scoble 1992). Sodium is necessary for successful reproduction, so adult Lepidoptera often need to obtain it in other ways (Zaspel 2012). The liquid substrate appears to be irrelevant; Boggs and Dau 2004 indicate that many adult Lepidoptera are stimulated to feed by a need to replenish sodium. Although Boggs and Dau did not study any of the Lepidoptera that feed on humans, their claims are supported by the observations of Büttiker 1997 and Zaspel (2012).

Blood‐feeding is evolutionarily distinct from sweat and tear‐feeding. In Lepidoptera, the skin‐piercing and hematophagous behaviors are believed to have evolved from the fruit‐piercing behaviors seen in closely‐related moths (Zaspel 2012). In contrast, lachryphagous behaviors are derived from behavior known as ‘puddling’: acquiring liquid from moist soil at the margins of small mud puddles (Downes 1973). Tear‐feeding Lepidoptera can land on a larger animal and essentially puddle around its eye, thus providing them with increased protection against predation. Some butterflies are known to puddle around animal dung and carrion (Boggs and Dau 2004, Downes 1973). For this reason, Boggs and Dau 2004 consider sweat‐feeding behavior a subset of puddling; dried sweat is likely to be present at puddling sites with carrion.

Sweat‐feeding moths Some hematophagous and lacryphagous Lepidoptera have been observed to also feed on sweat, however, these sweat‐feeding events are much shorter in duration than feeding events on other human fluids (Bänzinger 1992, Büttiker et al. 1996, Zaspel 2007). It is likely that sweat is not their primary source of sodium. In this paper, the category of ‘sudophagous Lepidoptera’ refers to sweat‐feeding Lepidoptera that do not use blood or tears as a primary source of sodium. It must be noted, however, that even sudophagous Lepidoptera may not use sweat as their primary source of sodium; sweat‐feeding is very similar to puddling, so it is possible that sudophagous Lepidoptera have no problem puddling in the absence of a sweaty animal. Collenette (1934) was the only one to specifically study lepidopteran attraction to sweat, as opposed to other sources of sodium. According to Collenette, at least eight families of Lepidoptera have sudophagous species. While collecting in Brazil, Collenette counted the specimens attracted to human perspiration in the absence of light and compared that number to specimens attracted to light, presumably in the absence of perspiration. This experimental design was probably flawed, since Collenette was unable to create a sweat‐free collecting area in his study. Collenette also did not provide species identifications for the moths. However, he found representatives of Noctuidae, Erebidae, Notodontidae, Geometridae, Uraniidae, Drepanidae, Pyralidae, and Crambidae, as well as two specimens of unidentified ‘microlepidoptera’. These families were also attracted to light. Limacodidae was notably absent; Collenette observed 66 specimens of Limacodidae at light, but none were attracted to sweat. This result correlates to limacodid morphology; Limacodidae have stunted probosces and cannot easily imbibe liquid, so they are unlikely to have evolved an attraction to a food source they can't utilize (Collenette 1934). Since puddling Lepidoptera may feed on sweat found near carrion, any families with species exhibiting puddling behavior should be considered as potentially sudophagous (Boggs and Dau, 2004). Downes (1973) observed four families of butterflies puddling in Colorado, as well as Pterophoridae and Tortricidae. There is also anecdotal evidence of African and Asian Sphingidae consuming “mammalian fluids off of the ground” (Bänziger 1992). Since puddling Lepidoptera can be found worldwide, it is likely, though not proven, that sudophagy is present globally in Lepidoptera. When Lepidoptera take sweat directly from humans, the feeding is only minimally invasive. The moth simply grazes its proboscis against the skin in order to lap up sweat from the human host; although these moths may take advantage of sweat from a preexisting wound, they will not create new wounds in the process of feeding (Bänziger and Büttiker 1969, Zaspel 2007).

Tear‐feeding moths Before discussing the lachryphagous moths in detail, the distinction between “tear‐feeding” and “eye‐frequenting” moths should be clarified. Though these terms are sometimes used interchangeably, they are not identical. Some moths will consume tears, but not directly from the eye. For example, the sweat‐feeding Sphingidae cited by Bänziger 1992 are likely to consume many types of body fluids from the ground, including tears. Currently, all moths known to place their proboscis on an eye do so with the intent of feeding on tears, but there may be a species discovered in the future that frequents the eye without feeding. Thus, the semantic distinction between tear‐feeding and eye‐frequenting should be maintained. Eye‐frequenting behavior in moths was first observed in 1852, on cows in South Africa (Büttiker 1997). Since then, lachryphagous eye‐frequenting moths have also been seen in Western Africa, Madagascar, Southeast Asia, South America, Central America, and Mexico (Bänziger and Büttiker 1969, Büttiker 1997, Selman 1972). There is also a single documented U.S. record: Selman (1972) observed multiple specimens of the geometrid moth Euchlaena pectinaria feeding near the eyes of a horse. In addition to Geometridae, species of eye‐frequenting lachryphages are present in Nymphalidae, Noctuidae, Notodontidae, Crambidae, Drepanidae (in subfamily Thyatirinae), and Sphingidae (Bänziger 1992, Downes 1973). Tear‐feeding is primarily observed on relatively large mammals, such as cattle, horses, oxen, deer, and elephants (Bänziger and Büttiker 1969). There are only a couple instances of non‐mammalian vertebrates being used as hosts. For example, the nymphalid tear‐feeders were observed frequenting the eyes of caimans and turtles in South America (Downes 1973), and a single noctuid species, Hemiceratoides hieroglyphica, was seen on two species of bird in Madagascar (Hilgartner et al. 2007). Many of the species feeding on human tears also feed on the tears of other mammals; there is no species known to feed exclusively on human tears. In total, approximately 110 lachryphagous species have been observed to frequent the eyes of animals, and 23 of these species have been observed feeding on humans (Büttiker et al. 1996). Feeding behavior of lachryphagous moths is only partially understood. Selman (1972) indicates that tear‐feeders attempt to select the host with the most watery eyes in order to obtain the greatest amount of tears. However, Bänziger and Büttiker (1969) believe that the eye‐frequenting moths induce watery eyes by causing irritation with the proboscis. Ideally, the proboscis would stimulate tear production without causing the host to blink and shut its eye. When feeding on humans, many eye‐frequenters tend to crawl around the face and probe other orifices with the proboscis before finally placing the proboscis on the open eye. Bänziger and Büttiker (1969) believe this is evidence of the moth's initial inability to locate the eye. The moth is likely thrown off by sodium present in the nose and mouth, as well as sodium from sweat. If this is true, it implies that the moth might also be interested in taking in sodium from human saliva or mucus, though this has never been documented. Bänziger and Büttiker (1969) provided images of eye‐frequenting moths in the process of feeding on humans. These images imply that moths of different families take different approaches to tear‐feeding based on their particular morphology. For example, the crambid tear‐feeder Filodes fulvidorsalis stands relatively far from the eye while feeding. This may be due to a long proboscis, but it is also due to wing orientation. Crambidae tend to spread their wings while at rest, so if they stand too close to the eye, the wings will likely cause unwanted irritation. When irritated, the human host is more likely to remove the moth. In contrast, geometrid tear‐feeders, such as Hypochrosis hyadaria, stand very close to the eye while feeding. These Geometridae keep their wings elevated when at rest, thus, they are less likely to make contact with the human eye. Many species of Geometridae cannot elevate their wings when at rest, but Adler (1982) observed elevated wings in 80% of all geometrids that were seen puddling. This implies a correlation between resting wing position and predisposition to puddling behavior, and consequently, tear‐feeding behavior. Rhagastis olivacea, the only known sphingid eye‐frequenter, is very large and has large spines on its legs; it is unlikely to land on a human without causing noticeable pain. Instead of landing, R. olivacea hovers in the air while extending its long proboscis toward the eye, in order to feed on the human with minimal interference (Bänziger 1992). Interestingly, almost all moths observed feeding on tears are males. Although the sodium in tears is necessary for them to successfully reproduce, it is likely that the males accumulate sodium and then transfer it to the female during mating, thus, the female may not need to collect sodium on her own (Boggs and Dau 2004, Zaspel 2012). Only two species of tear‐feeders, the Southeast Asian Noctuidae Arcyophora sylvatica and Lobocraspis griseifusa, appear to display significant amounts of females frequenting eyes to directly obtain sodium. Most eye‐frequenters are hemilachryphagous: They occasionally feed on tears, but will also obtain nutrients from other sources (Waage 1979). Only one species, L. griseifusa, is known to be eulachryphagous. It possesses multiple adaptations enabling it to exclusively feed on tears (Waage 1979). This moth has a relatively short proboscis and its wings are folded at rest; this enables multiple specimens to crowd around one eye simultaneously. As many as 12 have been observed feeding from a single cow eye at once (Bänziger 1992). This species is able to continue feeding even when its host closes its eye (Bänziger and Büttiker 1969). Most importantly, it is able to obtain all necessary nutrients from tears, not just sodium (Zaspel 2007). Specimens of L. griseifusa were found to have particular proteinases, not present in other tear‐feeders, which are capable of digesting some of the proteins found in tears (Scoble 1992). Hemiceratoides hieroglyphica was mentioned earlier because it uniquely feeds on bird tears. However, it is also unique among tear‐feeders because of its unusual proboscis morphology. Other tear‐feeders have smooth probosces, occasionally with very small spines (Zaspel 2011). Hemiceratoides hieroglyphica has a harpoon‐like proboscis with large barbs, spines, and sclerotized cuticular hooks (Hilgartner 2007). Curiously, it does not use these modifications to pierce the bird's eyelid; Hilgartner 2007 believes that the barbs help anchor the proboscis while the moth feeds. This enables feeding while the bird is sleeping by holding its proboscis precisely between the eyelids. The proboscis morphology of H. hieroglyphica greatly resembles that of the blood feeders (Zaspel 2011). This species is actually in the same subfamily (Noctuidae: Calpinae) as the blood‐feeders, so it is more closely related to hematophagous moths than lachryphagous moths.

Blood‐feeding moths As with lachryphages and eye‐frequenting moths, there is also a distinction between hematophages and skin‐piercing moths. A hematophage is defined by what it eats, while a skin‐piercer is defined by how it eats. With regards to Lepidoptera, this is strictly an issue of semantics that has not required clarification in previous literature; the only known species of hematophagous moths are also the only known skin‐piercing species, and vice‐versa. However, some Lepidoptera have been observed feeding at open wounds (Büttiker 1997, Downes 1973), Additionally, some blood has been detected in the stomachs of a few specimens of L. griseifusa, a non‐skin‐piercer (Bänziger and Büttiker 1969). Thus, there is some evidence of a hematophagous moth that does not pierce the skin of its host. The blood‐feeding, skin‐piercing moths are all in the genus Calyptra (Noctuidae: Calpinae). There are 17 species in the genus, but only ten species are definitively known as blood‐feeders; the other species are fruit‐piercing moths (Zaspel 2012). However, all species of Calyptra use fruit as an important source of nutrition. Some Calyptra have also been observed lapping sweat off of the host's skin after a feeding (Zaspel 2007). They are only found in the Old World, in parts of Europe, Africa, and Southeast Asia (Zaspel 2007). In addition to humans, they have been observed feeding on a variety of large mammals, including cattle, zebu, rhinoceros, and elephants (Zaspel 2012). As with most tear‐feeding moths, blood‐feeding is done exclusively by males, presumably for the same reason: female Calyptra obtain sodium directly from the male during mating (Zaspel 2012). Hematophagous moths have modified probosces that enable them to pierce even the toughest mammalian skin. The probosces vary somewhat among different species, but all of them have a combination of erectile barbs and tear‐shaped hooks on each galea (half of the proboscis) (Figure 1). In order to take a blood meal, the moth will use the tip of its proboscis to drill a small hole in the skin. Then, repeated antiparallel movements of the galeae enable the barbs and hooks to penetrate the host's skin and repeatedly pierce the blood vessels (Krenn 2010). This creates a subcutaneous pool of blood that can then be imbibed (Zaspel 2011, 2012). Unlike tear‐feeding moths, which are present in multiple families of Lepidoptera, the blood‐feeding moths in Calyptra do not appear to exhibit any variation in feeding behavior. Figure 1 Open in figure viewer PowerPoint Calyptra eustrigata. eb erectile barbs, feb furcate erectile barbs, sc sensory cone, th tearing hooks (From Zaspel et al. 2011 Proboscis of the blood‐feeding, skin‐piercing motherectile barbs,furcate erectile barbs,sensory cone,tearing hooks (From Zaspel et al.. Reprinted with permission from Zoomorphology).

Harmful health effects There are only two documented negative health effects caused by Lepidoptera feeding on mammals – localized irritation and localized inflammation. Only skin‐piercing and eye‐frequenting moths are known to be associated with these symptoms; there is no record of a sweat‐feeder causing irritation or inflammation by licking or lapping up moisture from mammalian skin. After a skin‐piercing moth feeds, the site of the wound reportedly undergoes “slight swelling” and there is a “slight stinging pain for 2–3 h following the attack” (Zaspel 2007). The eye‐frequenting moths cause irritation as they move their proboscis along the eye prior to feeding. Bänziger and Büttiker (1969) believe that the moth does this in order to stimulate tear production and increase rate of lachrymal flow. However, this hypothesis has not been tested; the probing movements may simply be the moth's attempts to find the optimal optical site for feeding. Among eye‐frequenting moths, L. griseifusa appears to cause the most pain in humans. Bänziger observed this first‐hand by allowing a single L. griseifusa to feed on him. Bänziger noticed that when he closed his eye during moth feeding, he would feel an “extremely sharp pain.” However, when his eye was open during feeding, he only felt “irritating stings of short duration” (Bänziger and Büttiker 1969). The extra pain associated with closed‐eye feeding might be the result of the shut eyelid making contact with minute triangular spines that on the surface of the L. griseifusa proboscis (Zaspel 2011). The threat of increased pain likely incentivizes hosts to keep their eyes open while L. griseifusa feeds; this increases the feeding surface area and enables greater numbers of moths to simultaneously feed on the same eye. In contrast to L. griseifusa, the sphingid R. olivacea does not cause any pain when placing its proboscis on the eye; Bänziger 1992 describes feeling only a “slightly mild [perception]…between the lower lid and the cornea.” However, during that same encounter, R. olivacea also placed its proboscis inside Bänziger's nostrils. This produced a tickling sensation that was harmless but highly irritating (Bänziger 1992). The thyatirine Chaeopsestis ludovicae is a tear‐feeder that is prone to hurt its host with its sharp tarsal claws. When it lands next to the eye to begin feeding, one or more of its tarsal claws has a tendency to scratch the conjunctiva, causing mechanical damage and irritation akin to a “grain of sand being rubbed between eye and lid” (Bänziger 1992). In one instance, the moth frequently moved its tarsus during feeding, increasing the amount of pain felt each time (Bänziger 1992). The proboscis of C. ludovicae did not cause any notable irritation. The symptoms produced by eye‐frequenting moths are similar to those in the condition called Ophthalmia nodosa – a reaction caused by contact with lepidopteran hairs or setae (Watson and Sevel 1966). However, the latter condition is sometimes exacerbated by toxins in the setae; lachryphagous moths do not transmit any toxins while feeding. Although it is theoretically possible for scales to fall off of a feeding moth onto the host's open eye, this would merely cause additional mechanical irritation. There are no adult lacryphagous moths with toxic or urticating setae.

Vector potential Hematophagous and lachryphagous Lepidoptera could potentially serve as vectors for disease, though this has never been documented (Bänziger 1992, Hilgartner 2007, Zaspel 2011). For successful biological transmission, a pathogen would most likely need to be in the vector's salivary gland, where it could multiply or change form and subsequently undergo transmission to the host via the vector's proboscis (Krenn and Aspock 2012). Disease agents present in the proboscis could also be mechanically transmitted during feeding. Bänziger and Büttiker (1969) hypothesize that a lachryphagous moth could feed at an animal's open wound and then move to the eye of a second animal, potentially transferring pathogens from the wound of the old host to the eye of the new host. If the moth tends to scratch the host with its tarsal claws while feeding, then pathogens on the legs could be mechanically transmitted through the small wounds. Bänziger and Büttiker (1969) claim that eye‐frequenting, lachryphagous moths may vector mammalian epidemic keratoconjunctivitis. However, no eye‐frequenting moth has ever demonstrated vector competence for any type of pathogen. Gouws 1995 showed that some bacteria found in cattle with ophthalmia, including Staphylococcus, were also present in the probosces of moths that were caught feeding on cattle tears. Although this implies that the moths may have transmitted harmful bacteria to the cattle, there was no conclusive evidence for transmission. Sudophagous Lepidoptera have never been considered potential disease vectors because they only make brief, non‐penetrative contact with host skin during feeding. This makes biological transmission impossible and mechanical transmission highly unlikely. However, Bänziger and Büttiker's open‐wound hypothesis for tear‐feeders could apply to sweat‐feeders as well. Out of all of the tear‐feeding moths, it is likely that H. hieroglyphica, the Malagasy moth that feeds on bird tears, would be the most competent vector for a disease agent. This species feeds when its host is sleeping, creating minimal disturbance and giving it an opportunity to feed for a long time – up to 35 min (Hilgartner 2007). This long feeding time has led Hilgartner 2007 to speculate that its saliva may contain some sort of anesthetic to prevent the host from waking up. By inserting its barbed proboscis through the eyelid into the eye, it has the opportunity for both biological and mechanical transmission. However, H. hieroglyphica would probably be unable to transmit diseases to humans. This species is specifically adapted to feeding on bird eyes because of the dearth of large mammals in Madagascar; its harpoon‐shape proboscis may be too specialized to feed on mammalian hosts without disturbing them (Hilgartner 2007). Compared to H. hieroglyphica, L. griseifusa has a much greater affinity for human tears. It is also able to continue feeding on the eye even when the eye is shut. These characters make L. griseifusa the most competent vector for a human disease. C. ludovicae, which has a tendency to scratch the human eyelid and conjunctiva with its tarsi, could also be a competent vector for mechanical transmission. The species that tend to probe additional orifices, such as the nose and ear, may also have increased vector competency. However, in all of these examples, the variables regarding a pathogen's ability to survive inside the moth, and find its way to the salivary gland or lower tarsi, are unknown. Although some blood‐feeders do not appear to feed on humans, the ones that do feed on humans do not exhibit notable variation in their feeding behavior (Zaspel 2007). Thus, all of the blood‐feeders that feed on humans appear to exhibit equal vector competency.

Prevention and control Since there is no known threat of disease from Lepidoptera that feed on human body fluids, there is no literature containing methods of protection. However, if one is interested in avoiding the ocular irritation caused by eye‐frequenting lachryphagous moths, the simplest option is to wear some sort of eye covering. Tear‐feeders are most likely to feed at night, when their hosts are sleeping or drowsy (Scoble 1992), so wearing a sleep mask, goggles, or even a pair of sunglasses could offer sufficient protection. A fire with heavy smoke has also been shown to repel tear‐feeding moths; Bänziger 1973 reports that some Thai farmers successfully use smoke to keep moths away from their livestock.