When we come across horses or cows, we often see them trying to get rid of the annoying insects that flutter around their eyes. What are they doing there? Are they looking for something? The next time you witness this phenomenon, remember this term: “lachryphagy”, because you are probably witnessing these insects trying to feed on tears.
Lachryphagy or feeding from tears is a widespread phenomenon among terrestrial arthropods. Most cases are known in the group of Lepidoptera (butterflies and moths), but there are also species of Diptera (such as some flies), Orthoptera (such as some grasshoppers) and Hymenoptera (bees) that manifest this behavior. The hosts are usually large mammals, including humans, large reptiles such as turtles and crocodiles, and some birds. Until recently, this behavior was restricted to arthropods with a proboscis, the tubular-shaped mouth appendage characteristic of flies and butterflies. Logically, this organ allows them to get close enough to the eye to absorb tears without disturbing the host and prevent it from reacting violently. However, science continues to discover new specimens of tear drinkers, some as unexpected as a cockroach. In 2019 it was possible to photograph in the Ecuadorian Amazon a specimen positioned on the head of a lizard (Anolis fuscoauratus) with its mouth over the reptile’s eye, presumably feeding on its tears (image below). It was a shocking find, partly because it is an insect without a proboscis, so it has to stick to the eye and risk its survival.
Lachryphagy is defined as a supplementary feeding, i.e., it would not be subject to the obtaining of energy and essential nutrients, but to the acquisition of specific micronutrients. Thus, specialists usually relate it to the behavior known as puddling. This habit consists of feeding on mud, excrement, carrion, and/or vertebrate secretions, including blood, sweat and tears. If you have ever seen a swarm of butterflies concentrated over a mud puddle or flies on excrement, you have witnessed this phenomenon. However, there is a slight nuance to be made, as some species acquire all the basic nutrients for their diets from these sources. These cases could not be considered puddling behaviors, because the target is not specific micronutrients. Puddling, therefore, refers to feeding in search of dietary supplements. And what kind of supplements? Mainly sodium (Na) and nitrogen (N), but also phosphorus, water or carbohydrates.
If you have tasted a tear, you will have noticed that it is salty. This is because one of its fundamental components is salt (NaCl). This is where lachryphagous insects obtain sodium, a fundamental element for the correct maintenance of blood pressure and neuromuscular activity, cell osmosis and the uptake of amino acids in the gut. It also plays an important role in reproduction. Nitrogen can be obtained by those insects that have proteases to digest the proteins contained in tears, because tears have high levels of proteins. It is also a determinant of reproductive success. Lachryphagy has been frequently observed in herbivorous and detritivorous insects. The diet of the former is usually poor in Na and that of the latter in N, so tears are a desirable resources.
What is the role of lachryphagy? Does it contribute to the survival of those who practice it? Does it improve their state of health? There are some clues to the functional utility of lachryphagy (and puddling in general). On the one hand, it has been observed that it is the males who perform this behavior in most of the species investigated. It is true that there are cases in which females are the ones searching for tears and others in which both sexes participate indistinctly, but this is not the norm. In the case of butterflies, some authors have suggested that males are the ones who mostly look for sources of Na because they need it more, since they are more active in flight than females. However, this hypothesis has hardly any support. Another clue is that there are hardly any records of lachryphagy or other types of puddling in the stages prior to sexual maturity. In short, these behaviors are mainly restricted to adult males (and thus capable of mating). Therefore, Na, N and other micronutrients obtained by puddling must be closely related to some activity exclusive to adults, such as reproduction, a hypothesis supported by the fact that puddling often precedes copulation.
Certainly, lachryphagy (and puddling) contribute to the survival of males, but also to improve their chances of having offspring, for example, by increasing the mobility of their sperm or helping them to maintain a healthy physiological state that allows them to compete with other males for access to females. However, they can also secure offspring by giving away these resources to females. This procedure is known as “nuptial gift”: males impregnate their spermatophores (capsules containing sperm) with these nutrients and give them to the female during mating. Once in the female, nutrients can follow various routes: replenish the nutritional losses derived from egg formation; be transferred to the larvae, so that they will be born with extra nutrients with which they can cope with nutritional deficiencies, ensure their survival at least until they acquire reproductive capacity and transmit their genes (and those of their parents) to the next generation… Therefore, lachryphagy (and puddling) would be determinant in assuring the reproductive success of these animals. In fact, there is evidence of better survival rates of larvae hatched from eggs provided with extra Na, as in the case of the butterfly Thymelicus lineola, although no such relationship has been found for other species that practice some kind of puddling. Moreover, there are studies that suggest that females of some species of insects that practice puddling are able to discriminate the males of better “quality” depending on the concentration of Na contained in their spermatophores. In this way, they could choose the spermatophore of the one that will guarantee the transmission of their genes for several generations.
Lachryphagy is usually classified within commensalism, that is, the ecological relationship in which one of the participants obtains benefits while the other is neither harmed nor benefited, although it can sometimes border on parasitism when the host suffers damage or disturbance, which can range from mere eye irritation to the transmission of bacterial or nematode infections, such as the dreaded thelaziasis.
I mentioned earlier that humans can be hosts to some lachryphagous insects. Indeed, a group of bees, the meliponines, also known as stingless bees, is known to have several representatives that are strongly attracted to human tears (e.g., Lisotrigona cacciae, L. furva or Pariotrigona klossi), although they also visit other mammals. Bee workers are responsible for collecting tears, visiting human eyes individually or in swarms of 5-7 individuals. They are likely to help each other find eyes by leaving pheromone trails. In this way, they are able to locate an eye even if it is closed. It is thought that, in addition to water, these insects consume tears to obtain amino acids and salts. They also seem to have suffered the loss or reduction of some traits to optimize their lachryphagous behavior, for example: they rarely visit flowers, have a small amount of pollen or resin on body or legs, reduced pilosity, etc. All this suggests a trade-off: they obtain micronutrients mainly from tears rather than from flowers, so the traits that facilitated their interaction with flowers have been reduced or lost as they lose their usefulness. This would also have a positive impact on lachryphagy, as high pilosity or amount of resin could cause irritation to the host or the insect to be trapped between the eyelashes.
Lachryphagous invertebrates usually exhibit characteristics that maximize the benefits obtained from lachryphagy. These adaptations make it possible to remain as long as possible on the eye of the host without attracting its attention or disturbing it. For instance, the moth Filodes fulvidorsalis tries to ingest tears from a distance, without getting too close to the eyes. This is possible because it has a very long proboscis. Moreover, it is convenient for it to do so, since, when it is perched, it tends to keep its wings spread, with the danger of coming into contact with the host’s eye and irritating it. Hypochoris hyadaria, on the other hand, may come closer to the eyes. Like other members of its family, it tends to keep its wings elevated when at rest, thus avoiding the risk of disturbing the host. Rhagostis olivacea, a large butterfly with abundant pilosity on its legs, tries to interfere as little as possible by gliding around the eye and extending its proboscis without landing.
REFERENCES
Bänzinger, H., Boongird, S., Sukumalanand, P., Bänzinger, S. (2009). Bees (Hymenoptera: Apidae) that drink human tears. J. Kans. Entomol. Soc. 82, 135-150. https://doi.org/10.2317/JKES0811.17.1
De la Rosa, C.L. (2014). Additional observations of lachryphagous butterflies and bees. Front. Ecol. Environ. 12, 210-210.
Molleman, F. (2010). Puddling: from natural history to understanding how it affects fitness. Entomol. Exp. Appl. 134, 107-113. https://doi.org/10.1111/j.1570-7458.2009.00938.x
Plotkin, D., Goddard, J. (2013). Blood, sweat, and tears: a review of the hematophagous, sudophagous, and lachryphagous Lepidoptera. J. Vector Ecol. 38, 289-294. https://doi.org/10.1111/j.1948-7134.2013.12042.x
Raloff, J. (2014). These insects thirst for tears. Science News for Students [online] May 1, available in: https://www.sciencenewsforstudents.org/article/these-insects-thirst-tears
Van den Burg, M.P., González de Rueda, J.A. (2021). Lachryphagy by cockroaches: reptile tears to increase reproductive output? Neotrop. Biodivers. 7, 276-278. https://doi.org/10.1080/23766808.2021.1953892
