Pyrrolizidine alkaloid sequestration
Encyclopedia
Pyrrolizidine alkaloid sequestration by insect
s is done for defense
and mating purposes. Various species of insects have been known to utilize molecular compounds from plants for their own defense and even as their pheromone
s or precursors to their pheromones. A few Lepidoptera
have been found to sequester chemicals from plants which they retain throughout their life and Arctiidae
is no exception to this strategy. Starting in the mid-twentieth century researchers investigated various members of Arctiidae, and how these insects sequester pyrrolizidine alkaloids (PA’s) during their life stages, and utilize these chemicals as adults for pheromones or pheromone precursors. PA’s are also used by members of the Arctiidae for defense against predators throughout the life of the insect.
Pyrrolizidine alkaloids are a group of chemicals produced as secondary plant metabolites, all of which contain a pyrrolizidine nucleus. This nucleus is made up of two pyrrol rings bonded by one carbon and one nitrogen. There are two forms in which PA’s can exist and will readily interchange between: a pro-toxic free base form, also called a tertiary amine
, or in a non-toxic form of N-oxide.
Researchers have collected data that strongly suggests that PA’s can be registered by taste receptor
s of predators, acting as a deterrent from being ingested. Taste receptors are also used by the various moth
species that sequester PA’s, which often stimulates them to feed. As of 2005, all of the PA sequestering insects that have been studied have all evolved a system to keep concentrations of the PA pro-toxic form low within the insect’s tissues.
Researchers have found a number of Arctiidae that utilize PA’s for protection and for male pheromones or precursors of the male pheromones, and some studies have found evidence suggesting PA’s have behavioral and developmental effects. Estigmene acrea
, Cosmosoma myrodora, Utetheisa ornatrix, Creatonotos gangis
and Creatonotos transiens
are all members of the family Arctiidae and found to use PA’s for their defense and/or male pheromones. Parsimony suggests that the sequestering of PA’s in the larval stage evolved in the subfamily Arctiinae common ancestor. The loss of ability to sequester and utilize PA’s has occurred in a number of species, along with the switch from larval uptake to adult uptake of PA’s occurring multiple times within the Arctiinae taxon.
Members of Arctiidae
typically sequester PA’s from their diets, but sometimes must specifically ingest fluids excreted by plants that are not a part of their diets. Sequestered PA’s are kept in various tissues and varying concentration which is dependent upon the species. PA’s are found in the cuticle
of all studied Arctiidae
mentioned here, but some also package these chemicals into their spermatophore
s as seen in Creatonotos gangis
and Creatonotos transiens
. The display of PA’s on the exoskeleton
is believed to cue predators to the unpalatability of the prey.
Eisner and Eisner looked at the palatability of PA positive and negative U. ornatrix to wolf spiders, Lycosa ceratiola, in both the larval form and adult form. They found that the pyrrolizidine positive organisms were typically released unharmed by spiders except in two field circumstances where the larva were probably envenomated prior to spider’s release and died two days after the attack. All of the PA negative organisms were eaten by spiders. These findings were in line with prior studies done by Eisner and Meinwald which looked at orb weavers and U. ornatrix, along with spiders being fed beetle
larva covered in PA’s, which they rejected. All of these findings support PA’s being utilized for defense against predation.
Studies have further elucidated the defenses and uses of PA’s in Arctiidae. One study researched C. myrodora and how PA’s protect this species from spider predation among other things. It found that PA’s ingested from fluids excreted by plants aided in defense from predation. All organisms permitted access to PA containing diets that were fed to spiders were cut loose from the webs. Interestingly, females that had PA deprived diets, but allowed to mate with PA positive males, were also released from the spider’s webs. Further observations showed that male C. myrodora have a pair of pouches where they produce PA laden filaments, which are typically released over the female prior to copulation as a nuptial gift. Experiments show that the filaments give the females more PA’s, explaining why spiders released mated PA negative females from their webs. Most of the PA’s from the males were subsequently transferred to the eggs when deposited. Three clusters of eggs that were laid after copulation with a PA positive male all tested positive for alkaloids and the one cluster that resulted from a PA negative male copulation tested negative. By the eggs getting a dose of PA’s, the authors suggest that the eggs are being protected from predators such as Coccinelidae beetles.
Jordan and others’ study found a very interesting effect of the larval ingestion of PA’s. Male Estigmene acrea
moths that consumed PA’s in their diet as larvae produced hydroxydanaidal, a volatile PA compound, and displayed their coremata
: a bifid, inflatable male-specific organ, utilized in dispersing pheromones in the adult stage. Larvae that were fed diets without PA’s rarely displayed their coremata and did not produce hydroxydanaidal. E. acrea have been observed in the wild displaying their coremata, an activity which attracts both males and females and is known as lekking. Lekking was described by Willis and Birch in 1982, but larvae raised in the laboratory prior to this study rarely engaged in lekking or corematal displays. Scientists were unsure of why this phenomenon didn’t occur in the lab, but laboratory raised larvae were usually reared on commercially available food which lacks PA’s. The authors suggest that the PA’s are used by the males to attract other moths by releasing the volatile PA hydroxydanaidal into the air. It is suggested in this study that this strategy of mate attraction came about by tapping into the PA affinity already programmed into the moths for feeding, which is further supported by the observation that E. acrea females release their pheromones a little bit later in the evening than the males.
Similar uses of coremata to attract other moths have been observed in C. gangis and C. transiens along with altered development of coremata when larvae are reared without PA’s. Boppre and Schneider observed adult males of these two species that were not permitted to eat PA’s. Their coremata only developed into two, stalk-like projections with very few hairs arising from these stalks. Males that were given plants that produced PA’s to feed upon, developed long coremata with four tubes, each longer than the males body, and each tube was highly pubescent. The authors suggest from this observation that there is a basic corematal phenotype, the two stalked coremata, and that PA’s are required to form full coremata which is much larger and more elaborate than the basic corematal expression. These observations were further investigated by feeding larvae different amounts of PA’s which had a direct correlation to the development of the coremata, which reached a maximum plateau around 2 mg of PA’s ingested while in larval form. Similar to Jordan and others’ findings, the males raised on a diet devoid of PA’s did not produce hydroxydanaidal.
Insect
Insects are a class of living creatures within the arthropods that have a chitinous exoskeleton, a three-part body , three pairs of jointed legs, compound eyes, and two antennae...
s is done for defense
Defense in insects
Insects have a wide variety of predators, including birds, reptiles, amphibians, mammals, carnivorous plants, and other arthropods. The great majority of individuals born do not survive to reproductive age, with perhaps 50% of this mortality rate attributed to predation. In order to deal with this...
and mating purposes. Various species of insects have been known to utilize molecular compounds from plants for their own defense and even as their pheromone
Pheromone
A pheromone is a secreted or excreted chemical factor that triggers a social response in members of the same species. Pheromones are chemicals capable of acting outside the body of the secreting individual to impact the behavior of the receiving individual...
s or precursors to their pheromones. A few Lepidoptera
Lepidoptera
Lepidoptera is a large order of insects that includes moths and butterflies . It is one of the most widespread and widely recognizable insect orders in the world, encompassing moths and the three superfamilies of butterflies, skipper butterflies, and moth-butterflies...
have been found to sequester chemicals from plants which they retain throughout their life and Arctiidae
Arctiidae
Arctiidae is a large and diverse family of moths with around 11,000 species found all over the world, including 6,000 neotropical species. This family includes the groups commonly known as tiger moths , which usually have bright colours, footmen , lichen moths and wasp moths...
is no exception to this strategy. Starting in the mid-twentieth century researchers investigated various members of Arctiidae, and how these insects sequester pyrrolizidine alkaloids (PA’s) during their life stages, and utilize these chemicals as adults for pheromones or pheromone precursors. PA’s are also used by members of the Arctiidae for defense against predators throughout the life of the insect.
Pyrrolizidine alkaloids are a group of chemicals produced as secondary plant metabolites, all of which contain a pyrrolizidine nucleus. This nucleus is made up of two pyrrol rings bonded by one carbon and one nitrogen. There are two forms in which PA’s can exist and will readily interchange between: a pro-toxic free base form, also called a tertiary amine
Amine
Amines are organic compounds and functional groups that contain a basic nitrogen atom with a lone pair. Amines are derivatives of ammonia, wherein one or more hydrogen atoms have been replaced by a substituent such as an alkyl or aryl group. Important amines include amino acids, biogenic amines,...
, or in a non-toxic form of N-oxide.
Researchers have collected data that strongly suggests that PA’s can be registered by taste receptor
Taste receptor
A Taste receptor is a type of receptor which facilitates the sensation of taste.Examples include TAS2R16 and TAS2R38.They are divided into two families:* Type 1, sweet, first characterized in 2001: –...
s of predators, acting as a deterrent from being ingested. Taste receptors are also used by the various moth
Moth
A moth is an insect closely related to the butterfly, both being of the order Lepidoptera. Moths form the majority of this order; there are thought to be 150,000 to 250,000 different species of moth , with thousands of species yet to be described...
species that sequester PA’s, which often stimulates them to feed. As of 2005, all of the PA sequestering insects that have been studied have all evolved a system to keep concentrations of the PA pro-toxic form low within the insect’s tissues.
Researchers have found a number of Arctiidae that utilize PA’s for protection and for male pheromones or precursors of the male pheromones, and some studies have found evidence suggesting PA’s have behavioral and developmental effects. Estigmene acrea
Estigmene acrea
The Salt Marsh Moth or Acrea Moth is a North American moth in the family Arctiidae.-Description:The head and thorax are white with the abdomen being yellow-orange with a row of black spots. The fore wing is white with a variable amount of black spots . The hind wing is yellow-orange in males and...
, Cosmosoma myrodora, Utetheisa ornatrix, Creatonotos gangis
Creatonotos gangis
Creatonotos gangis is a species of arctiid moth found in South East Asia and Australia.-Description and life cycle:Adults have white hindwings, and brown forewings, each with a dark streak, and a wingspan of . The abdomen is red or, more rarely, yellow. The eggs are yellow and round, and are laid...
and Creatonotos transiens
Creatonotos transiens
Creatonotos transiens is a moth of the Arctiidae family. It is found in China , Japan , eastern Afghanistan, Pakistan, India, Bangladesh, Nepal, Bhutan, Burma, Indochina, the Philippines, Borneo, Sulawesi and Lombok.The larvae feed on a wide range of...
are all members of the family Arctiidae and found to use PA’s for their defense and/or male pheromones. Parsimony suggests that the sequestering of PA’s in the larval stage evolved in the subfamily Arctiinae common ancestor. The loss of ability to sequester and utilize PA’s has occurred in a number of species, along with the switch from larval uptake to adult uptake of PA’s occurring multiple times within the Arctiinae taxon.
Members of Arctiidae
Arctiidae
Arctiidae is a large and diverse family of moths with around 11,000 species found all over the world, including 6,000 neotropical species. This family includes the groups commonly known as tiger moths , which usually have bright colours, footmen , lichen moths and wasp moths...
typically sequester PA’s from their diets, but sometimes must specifically ingest fluids excreted by plants that are not a part of their diets. Sequestered PA’s are kept in various tissues and varying concentration which is dependent upon the species. PA’s are found in the cuticle
Cuticle
A cuticle , or cuticula, is a term used for any of a variety of tough but flexible, non-mineral outer coverings of an organism, or parts of an organism, that provide protection. Various types of "cuticles" are non-homologous; differing in their origin, structure, function, and chemical composition...
of all studied Arctiidae
Arctiidae
Arctiidae is a large and diverse family of moths with around 11,000 species found all over the world, including 6,000 neotropical species. This family includes the groups commonly known as tiger moths , which usually have bright colours, footmen , lichen moths and wasp moths...
mentioned here, but some also package these chemicals into their spermatophore
Spermatophore
A spermatophore or sperm ampulla is a capsule or mass created by males of various animal species, containing spermatozoa and transferred in entirety to the female's ovipore during copulation...
s as seen in Creatonotos gangis
Creatonotos gangis
Creatonotos gangis is a species of arctiid moth found in South East Asia and Australia.-Description and life cycle:Adults have white hindwings, and brown forewings, each with a dark streak, and a wingspan of . The abdomen is red or, more rarely, yellow. The eggs are yellow and round, and are laid...
and Creatonotos transiens
Creatonotos transiens
Creatonotos transiens is a moth of the Arctiidae family. It is found in China , Japan , eastern Afghanistan, Pakistan, India, Bangladesh, Nepal, Bhutan, Burma, Indochina, the Philippines, Borneo, Sulawesi and Lombok.The larvae feed on a wide range of...
. The display of PA’s on the exoskeleton
Exoskeleton
An exoskeleton is the external skeleton that supports and protects an animal's body, in contrast to the internal skeleton of, for example, a human. In popular usage, some of the larger kinds of exoskeletons are known as "shells". Examples of exoskeleton animals include insects such as grasshoppers...
is believed to cue predators to the unpalatability of the prey.
Eisner and Eisner looked at the palatability of PA positive and negative U. ornatrix to wolf spiders, Lycosa ceratiola, in both the larval form and adult form. They found that the pyrrolizidine positive organisms were typically released unharmed by spiders except in two field circumstances where the larva were probably envenomated prior to spider’s release and died two days after the attack. All of the PA negative organisms were eaten by spiders. These findings were in line with prior studies done by Eisner and Meinwald which looked at orb weavers and U. ornatrix, along with spiders being fed beetle
Beetle
Coleoptera is an order of insects commonly called beetles. The word "coleoptera" is from the Greek , koleos, "sheath"; and , pteron, "wing", thus "sheathed wing". Coleoptera contains more species than any other order, constituting almost 25% of all known life-forms...
larva covered in PA’s, which they rejected. All of these findings support PA’s being utilized for defense against predation.
Studies have further elucidated the defenses and uses of PA’s in Arctiidae. One study researched C. myrodora and how PA’s protect this species from spider predation among other things. It found that PA’s ingested from fluids excreted by plants aided in defense from predation. All organisms permitted access to PA containing diets that were fed to spiders were cut loose from the webs. Interestingly, females that had PA deprived diets, but allowed to mate with PA positive males, were also released from the spider’s webs. Further observations showed that male C. myrodora have a pair of pouches where they produce PA laden filaments, which are typically released over the female prior to copulation as a nuptial gift. Experiments show that the filaments give the females more PA’s, explaining why spiders released mated PA negative females from their webs. Most of the PA’s from the males were subsequently transferred to the eggs when deposited. Three clusters of eggs that were laid after copulation with a PA positive male all tested positive for alkaloids and the one cluster that resulted from a PA negative male copulation tested negative. By the eggs getting a dose of PA’s, the authors suggest that the eggs are being protected from predators such as Coccinelidae beetles.
Jordan and others’ study found a very interesting effect of the larval ingestion of PA’s. Male Estigmene acrea
Estigmene acrea
The Salt Marsh Moth or Acrea Moth is a North American moth in the family Arctiidae.-Description:The head and thorax are white with the abdomen being yellow-orange with a row of black spots. The fore wing is white with a variable amount of black spots . The hind wing is yellow-orange in males and...
moths that consumed PA’s in their diet as larvae produced hydroxydanaidal, a volatile PA compound, and displayed their coremata
Coremata
Coremata is a genus of moths of the Crambidae family....
: a bifid, inflatable male-specific organ, utilized in dispersing pheromones in the adult stage. Larvae that were fed diets without PA’s rarely displayed their coremata and did not produce hydroxydanaidal. E. acrea have been observed in the wild displaying their coremata, an activity which attracts both males and females and is known as lekking. Lekking was described by Willis and Birch in 1982, but larvae raised in the laboratory prior to this study rarely engaged in lekking or corematal displays. Scientists were unsure of why this phenomenon didn’t occur in the lab, but laboratory raised larvae were usually reared on commercially available food which lacks PA’s. The authors suggest that the PA’s are used by the males to attract other moths by releasing the volatile PA hydroxydanaidal into the air. It is suggested in this study that this strategy of mate attraction came about by tapping into the PA affinity already programmed into the moths for feeding, which is further supported by the observation that E. acrea females release their pheromones a little bit later in the evening than the males.
Similar uses of coremata to attract other moths have been observed in C. gangis and C. transiens along with altered development of coremata when larvae are reared without PA’s. Boppre and Schneider observed adult males of these two species that were not permitted to eat PA’s. Their coremata only developed into two, stalk-like projections with very few hairs arising from these stalks. Males that were given plants that produced PA’s to feed upon, developed long coremata with four tubes, each longer than the males body, and each tube was highly pubescent. The authors suggest from this observation that there is a basic corematal phenotype, the two stalked coremata, and that PA’s are required to form full coremata which is much larger and more elaborate than the basic corematal expression. These observations were further investigated by feeding larvae different amounts of PA’s which had a direct correlation to the development of the coremata, which reached a maximum plateau around 2 mg of PA’s ingested while in larval form. Similar to Jordan and others’ findings, the males raised on a diet devoid of PA’s did not produce hydroxydanaidal.