Kleptopharmacophagy

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A group of danaine butterflies feeding on the caterpillar of Idea blanchardii blanchardii. From left to right: Euploea algea kirbyi, Ideopsis juventa tontoliensis, Danaus ismare ismare. Danaine kleptopharmacophagy.jpg
A group of danaine butterflies feeding on the caterpillar of Idea blanchardii blanchardii. From left to right: Euploea algea kirbyi, Ideopsis juventa tontoliensis, Danaus ismare ismare.

Kleptopharmacophagy is a term used for describing the ecological relationship between two different organisms, where the first is stealing the second's chemical compounds and consuming them. [1] [2] This scientific term was proposed by Australian, Singaporean, and American biologists in September 2021 in an article that was published in the journal Ecology by the Ecological Society of America. [3] [4] The phenomenon was first noticed in milkweed butterflies that were attacking caterpillars and drinking their internal liquid, proposedly to obtain toxic alkaloids used for defense, as well as for mating purposes. [5]

Contents

Characteristics

Kleptopharmacophagy is a generic term and a scientific neologism, that is used to describe the phenomenon of chemical theft between living organisms. [1] This special type of behavior is something new for researchers, as it does not match the traditional descriptions of biological interaction. [5] Kleptopharmacophagy cannot be defined simply with a use of classical ecological relationships and their descriptions, such as predation, parasitism and mutualism. [1] Besides being an interspecific interaction, kleptopharmacophagy can also be seen as a cannibalizing act (hence an intraspecific act), [4] with adults attacking larvae of their own species. [6] [7]

In butterflies

Kleptopharmacophagy was first observed in milkweed butterflies. Here a male Ideopsis vitrea vitrea is seen scratching and feeding on the caterpillar of Idea blanchardii blanchardii. Ideopsis vitrea kleptopharmacophagy.jpg
Kleptopharmacophagy was first observed in milkweed butterflies. Here a male Ideopsis vitrea vitrea is seen scratching and feeding on the caterpillar of Idea blanchardii blanchardii.

Kleptopharmacophagy has only been reported for butterflies in the subfamily Danainae, more commonly known as the milkweed butterflies. The phenomenon was first described in butterflies that were observed scratching and feeding on live larvae of other milkweed butterflies. [3] The initial discovery was made in year 2019 in forests of North Sulawesi, in Indonesia, when two researchers noticed that milkweed butterflies of different species, [2] [6] well-known for their toxicity and bright warning colours (aposematism), [3] were interacting with the larval stages of other butterflies. [2] [6] The adult insects were attacking and harassing the caterpillars by scratching at them with tarsal claws on their legs. [2] The butterflies then imbibed the juices from the wounded caterpillars with their long and curved proboscis. [6] Caterpillars that were targeted appeared to range from living to dead and dying individuals. Live caterpillars were observed to contort their bodies in an attempt to deter scratching, but usually succumbed to the repeat harassment. [2] [6]

There is also one recorded example of kleptopharmachophagy occurring between two adult butterflies; a male Ideopsis vitrea vitrea was feeding on a liquid, oozing from the wings of the male I. blanchardii blanchardii. [8]

Role

Parantica algeoides algeoides feeding on a dead arctiine moth. Arctiine moths are known to be chemically defended by pyrrolizidine alkaloids. In cases where the carcasses of alkaloid containing insects are preferred, the term necropharmacophagy may be more applicable. Parantica algeoides necropharmacophagy.jpg
Parantica algeoides algeoides feeding on a dead arctiine moth. Arctiine moths are known to be chemically defended by pyrrolizidine alkaloids. In cases where the carcasses of alkaloid containing insects are preferred, the term necropharmacophagy may be more applicable.

It is thought that such chemical theft serves at least two roles. By feeding on toxic caterpillars, the adult butterflies acquire additional toxins, which serve as a protection against predation. The stolen toxins, mostly pyrrolizidine alkaloids (PAs), are also of great importance for male butterflies, which use those compounds for producing mating pheromones. Additionally such chemicals are components of so-called nuptial gifts, consisting of male sperm and some nutrients, that are given from males to females during mating. Significance of the alkaloid use for male butterflies can be demonstrated through observation of male danaine butterflies congregating in large numbers at alkaloid producing plants, where they spend hours fervently scratching and liberating plant juices. [2]

Similar behaviour

Milkweed butterflies have also been previously seen feasting on some moribund pyrgormorphid grasshoppers, that are known to contain toxic alkaloids, [2] [8] [9] as well as obtaining desired chemicals from carcasses of dead insects of different taxa. Note that in this case, the term necropharmacophagy may be more appropriate, since butterflies feed on the dead animals. [8]

Similar behavior was observed with adult butterflies scratching leaves of different plants that possess various toxins in their vegetative organs (so-called leaf-scratching [6] ). Adult male danaine butterflies use their sharp tarsal claws to scratch and damage leaves of plants that contain high levels of pyrrolizidine alkaloids, thereby liberating the juices for consumption. [2] [10] Since kleptopharmacophagy was recorded and described only a few times, [4] it is thought that obtaining such chemicals by feeding on plants with alkaloids is a common and more frequent way of stocking toxins. [6] Kleptopharmacophagy is proposed to be an alternative way of acquiring these chemicals. [5]

Related Research Articles

<span class="mw-page-title-main">Caterpillar</span> Larva of a butterfly or moth

Caterpillars are the larval stage of members of the order Lepidoptera.

<i>Asclepias tuberosa</i> Species of flowering plant

Asclepias tuberosa, commonly known as butterfly weed, is a species of milkweed native to eastern and southwestern North America. It is commonly known as butterfly weed because of the butterflies that are attracted to the plant by its color and its copious production of nectar.

<span class="mw-page-title-main">Monarch butterfly</span> Milkweed butterfly in the family Nymphalidae

The monarch butterfly or simply monarch is a milkweed butterfly in the family Nymphalidae. Other common names, depending on region, include milkweed, common tiger, wanderer, and black-veined brown. It is amongst the most familiar of North American butterflies and an iconic pollinator, although it is not an especially effective pollinator of milkweeds. Its wings feature an easily recognizable black, orange, and white pattern, with a wingspan of 8.9–10.2 cm (3.5–4.0 in). A Müllerian mimic, the viceroy butterfly, is similar in color and pattern, but is markedly smaller and has an extra black stripe across each hindwing.

<i>Asclepias</i> Genus of flowering plants

Asclepias is a genus of herbaceous, perennial, flowering plants known as milkweeds, named for their latex, a milky substance containing cardiac glycosides termed cardenolides, exuded where cells are damaged. Most species are toxic to humans and many other species, primarily due to the presence of cardenolides. However, as with many such plants, some species feed upon them or from them. The most notable of them is the monarch butterfly, which uses and requires certain milkweeds as host plants for their larvae.

<i>Heliotropium</i> Genus of flowering plants in the borage family Boraginaceae

Heliotropium is a genus of flowering plants in the heliotrope family, Heliotropiaceae. There are around 325 species in this almost cosmopolitan genus, which are commonly known as heliotropes. They are highly toxic to dogs and cats.

<i>Euploea core</i> Species of butterfly

Euploea core, the common crow, is a common butterfly found in South Asia to Australia. In India it is also sometimes referred to as the common Indian crow, and in Australia as the Australian crow. It belongs to the crows and tigers subfamily Danainae.

<i>Greta oto</i> Species of butterfly

Greta oto is a species of brush-footed butterfly and member of the subfamily Danainae, tribe Ithomiini, and subtribe Godyridina. It is known by the common name glasswing butterfly for its transparent wings, which allow it to camouflage without extensive coloration. In Spanish-speaking regions, it may also be referred to as espejitos, meaning "little mirrors" because of its transparent wings. The butterfly is mainly found in Central and northern regions of South America, with sightings as far north as Texas and as far south as Chile. While its wings appear delicate, the butterfly is able to carry up to 40 times its own weight. In addition to its wing physiology, the butterfly is known for behaviors such as long migrations and lekking. Greta oto closely resembles Greta andromica.

<i>Danaus chrysippus</i> Species of butterfly

Danaus chrysippus, also known as the plain tiger, African queen, or African monarch, is a medium-sized butterfly widespread in Asia, Australia and Africa. It belongs to the Danainae subfamily of the brush-footed butterfly family Nymphalidae. Danainae primarily consume plants in the genus Asclepias, more commonly called milkweed. Milkweed contains toxic compounds, cardenolides, which are often consumed and stored by many butterflies. Because of their emetic properties, the plain tiger is unpalatable to most predators. As a result, its colouration is widely mimicked by other species of butterflies. The plain tiger inhabits a wide variety of habitats, although it is less likely to thrive in jungle-like conditions and is most often found in drier, wide-open areas.

<span class="mw-page-title-main">Queen (butterfly)</span> Species of butterfly

The queen butterfly is a North and South American butterfly in the family Nymphalidae with a wingspan of 80–85 mm. It is orange or brown with black wing borders and small white forewing spots on its dorsal wing surface, and reddish ventral wing surface fairly similar to the dorsal surface. The ventral hindwings have black veins and small white spots in a black border. The male has a black androconial scent patch on its dorsal hindwings. It can be found in meadows, fields, marshes, deserts, and at the edges of forests.

<span class="mw-page-title-main">Butterfly gardening</span> Gardening to benefit butterflies

Butterfly gardening is a way to create, improve, and maintain habitat for lepidopterans including butterflies, skippers, and moths. Butterflies have four distinct life stages—egg, larva, chrysalis, and adult. In order to support and sustain butterfly populations, an ideal butterfly garden contains habitat for each life stage.

<span class="mw-page-title-main">Garden tiger moth</span> Species of moth

The garden tiger moth or great tiger moth is a moth of the family Erebidae. Arctia caja is a northern species found in the US, Canada, and Europe. The moth prefers cold climates with temperate seasonality, as the larvae overwinter, and preferentially chooses host plants that produce pyrrolizidine alkaloids. However, garden tiger moths are generalists, and will pick many different plants to use as larval host plants.

<span class="mw-page-title-main">Pyrrolizidine alkaloid</span> Class of chemical compounds

Pyrrolizidine alkaloids (PAs), sometimes referred to as necine bases, are a group of naturally occurring alkaloids based on the structure of pyrrolizidine. Pyrrolizidine alkaloids are produced by plants as a defense mechanism against insect herbivores. More than 660 PAs and PA N-oxides have been identified in over 6,000 plants, and about half of them exhibit hepatotoxicity. They are found frequently in plants in the Boraginaceae, Asteraceae, Orchidaceae and Fabaceae families; less frequently in the Convolvulaceae and Poaceae, and in at least one species in the Lamiaceae. It has been estimated that 3% of the world’s flowering plants contain pyrrolizidine alkaloids. Honey can contain pyrrolizidine alkaloids, as can grains, milk, offal and eggs. To date (2011), there is no international regulation of PAs in food, unlike those for herbs and medicines.

<span class="mw-page-title-main">Cardenolide</span> Chemical compound

A cardenolide is a type of steroid. Many plants contain derivatives, collectively known as cardenolides, including many in the form of cardenolide glycosides (cardenolides that contain structural groups derived from sugars). Cardenolide glycosides are often toxic; specifically, they are heart-arresting. Cardenolides are toxic to animals through inhibition of the enzyme Na+/K+‐ATPase, which is responsible for maintaining the sodium and potassium ion gradients across the cell membranes.

<span class="mw-page-title-main">Ithomiini</span> Tribe of butterflies in the subfamily Danainae

Ithomiini is a butterfly tribe in the nymphalid subfamily Danainae. It is sometimes referred to as the tribe of clearwing butterflies or glasswing butterflies. Some authors consider the group to be a subfamily (Ithomiinae). These butterflies are exclusively Neotropical, found in humid forests from sea level to 3000 m, from Mexico to Argentina. There are around 370 species in some 40–45 genera.

<i>Utetheisa ornatrix</i> Species of moth

Utetheisa ornatrix, also called the ornate bella moth, ornate moth, bella moth or rattlebox moth, is a moth of the subfamily Arctiinae. It is aposematically colored ranging from pink, red, orange and yellow to white coloration with black markings arranged in varying patterns on its wings. It has a wingspan of 33–46 mm. Moths reside in temperate midwestern and eastern North America as well as throughout Mexico and other parts of Central America. Unlike most moths, the bella moth is diurnal. Formerly, the bella moth or beautiful utetheisa of temperate eastern North America was separated as Utetheisa bella. Now it is united with the bella moth in Utetheisa ornatrix.

<span class="mw-page-title-main">Senecionine</span> Chemical compound

Senecionine is a toxic pyrrolizidine alkaloid isolated from various botanical sources. It takes its name from the Senecio genus and is produced by many different plants in that genus, including Jacobaea vulgaris. It has also been isolated from several other plants, including Brachyglottis repanda, Emilia, Erechtites hieraciifolius, Petasites, Syneilesis, Crotalaria, Caltha leptosepala, and Castilleja.

Pyrrolizidine alkaloidosis is a disease caused by chronic poisoning found in humans and other animals caused by ingesting poisonous plants which contain the natural chemical compounds known as pyrrolizidine alkaloids. Pyrrolizidine alkaloidosis can result in damage to the liver, kidneys, heart, brain, smooth muscles, lungs, DNA, lesions all over the body, and could be a potential cause of cancer. Pyrrolizidine alkaloidosis is known by many other names such as "Pictou Disease" in Canada and "Winton Disease" in New Zealand. Cereal crops and forage crops can sometimes become polluted with pyrrolizidine-containing seeds, resulting in the alkaloids contaminating flour and other foods, including milk from cows feeding on these plants.

<span class="mw-page-title-main">Hair-pencil</span> Pheromone signaling structures in lepidopteran males

Hair-pencils and coremata are pheromone signaling structures present in lepidopteran males. Males use hair-pencils in courtship behaviors with females. The pheromones they excrete serve as both aphrodisiacs and tranquilizers to females as well as repellents to conspecific males. Hair-pencil glands are stored inside the male until courtship begins, at which point they are forced out of the body by sclerotized levers present on the abdomen. Coremata are very similar structures. Their exact definition is confused by early descriptions but they are more specifically defined as the internal, glandular, eversible structures that bear the hair-pencils and can be voluntarily inflated with hemolymph or air.

<i>Creatonotos gangis</i> Species of arctiine moth in South East Asia and Australia

Creatonotos gangis, the Baphomet moth or Australian horror moth, is a species of arctiine moth in South East Asia and Australia. It was described by Carl Linnaeus in his 1763 Centuria Insectorum.

<span class="mw-page-title-main">Milkweed leaf beetle</span> Species of beetle

The milkweed leaf beetle is a species of leaf beetle from the family Chrysomelidae. It is round bodied, 8–11 mm in length with a black head and pronotum and bright orange to yellow elytra with variable mottled black patches. Its colored and shaped like a super-sized ladybird beetle even though the ladybird is in a different family, Coccinellidae. The larva is shaped much like the adult except with a small tail extension. Its color varies from bright orange to white with a gray to black pronotum and prominent black spots around its spiracles.

References

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  2. 1 2 3 4 5 6 7 8 Roth, Annie (2021-09-09). "Milkweed Butterflies Are More Murderous Than They Look". The New York Times. ISSN   0362-4331 . Retrieved 2021-09-10.
  3. 1 2 3 Tea, Yi-Kai; Wei, Jonathan Soong; Beaver, Ethan P.; Lohman, David J. (2021). "Kleptopharmacophagy? Milkweed butterflies scratch and imbibe from Apocynaceae-feeding caterpillars". Ecology. 102 (12): e03532. doi:10.1002/ecy.3532. ISSN   1939-9170. PMID   34496059.
  4. 1 2 3 "Aussie scientists observe cannibalism in butterflies". www.news.cn. Retrieved 2021-09-10.
  5. 1 2 3 "Butterflies feed on live young to steal chemicals for 'wedding gifts'". phys.org. Retrieved 2021-09-10.
  6. 1 2 3 4 5 6 7 "Butterflies feed on live young to steal chemicals for 'wedding gifts'". The University of Sydney. Retrieved 2021-09-10.
  7. "Cannibalistic butterflies chow down on live caterpillars". BBC Science Focus Magazine. Retrieved 2021-09-10.
  8. 1 2 3 "Kleptopharmacophagy? Milkweed butterflies scratch and imbibe from Apocynaceae‐feeding caterpillars". ResearchGate. Retrieved 2021-09-10.
  9. dmCl1ZgHPv. "Milkweed butterflies are deadlier than they look" . Retrieved 2021-09-10.{{cite web}}: CS1 maint: numeric names: authors list (link)
  10. Lawson, Nancy; Vane-Wright, Richard I.; Boppré, Michael (2021). "The puzzle of monarch butterflies (Danaus plexippus) and their association with plants containing pyrrolizidine alkaloids". Ecological Entomology. 46 (5): 999–1005. doi: 10.1111/een.13051 . ISSN   1365-2311.

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