Chemical ecology

Last updated

Chemical ecology is the study of chemically mediated interactions between living organisms, and the effects of those interactions on the demography, behavior and ultimately evolution of the organisms involved. It is thus a vast and highly interdisciplinary field. [1] [2] Chemical ecologists seek to identify the specific molecules (i.e. semiochemicals) that function as signals mediating community or ecosystem processes and to understand the evolution of these signals. The substances that serve in such roles are typically small, readily-diffusible organic molecules, but can also include larger molecules and small peptides. [3]

Contents

In practice, chemical ecology relies extensively on chromatographic techniques, such as thin-layer chromatography, high performance liquid chromatography, and gas chromatography, to isolate and identify bioactive metabolites. To identify molecules with the sought-after activity, chemical ecologists often make use of bioassay-guided fractionation. Today, chemical ecologists also incorporate genetic and genomic techniques to understand the biosynthetic and signal transduction pathways underlying chemically mediated interactions. [4]

Plant chemical ecology

Monarch butterfly caterpillar on milkweed plant. Monarch Butterfly Danaus plexippus Vertical Caterpillar 2000px.jpg
Monarch butterfly caterpillar on milkweed plant.

Plant chemical ecology focuses on the role of chemical cues and signals in mediating interactions of plants with their biotic environment (e.g. microorganisms, phytophagous insects, and pollinators).

Plant-insect interactions

Series from a study by Eisner and colleagues investigating defensive spray in bombardier beetles. The paper is specially treated to have a color reaction with the spray, which is normally clear. Chlaenius Plate 10 Eisner et al 1963.png
Series from a study by Eisner and colleagues investigating defensive spray in bombardier beetles. The paper is specially treated to have a color reaction with the spray, which is normally clear.

The chemical ecology of plant-insect interaction is a significant subfield of chemical ecology. [2] [5] [6] In particular, plants and insects are often involved in a chemical evolutionary arms race. As plants develop chemical defenses to herbivory, insects which feed on them evolve immunity to these poisons, and in some cases, repurpose these poisons for their own chemical defense against predators. For example, caterpillars of the monarch butterfly sequester cardenolide toxins from their milkweed host-plants and are able to use them as an anti-predator defense. Whereas most insects are killed by cardenolides, which are potent inhibitors of the Na+/K+-ATPase, monarchs have evolved resistance to the toxin over their long evolutionary history with milkweeds. Other examples of sequestration include the tobacco hornworm Manduca sexta , which use nicotine sequestered from tobacco plants in predator defense; [5] and the bella moth, which secretes a quinone-containing froth to deter predators obtained from feeding on Crotalaria plants as a caterpillar.

Chemical ecologists also study chemical interactions involved in indirect defenses of plants, such as the attraction of predators and parasitoids through herbivore-induced volatile organic compounds (VOCs).

Plant-microbe interactions

Plant interactions with microorganisms are also mediated by chemistry. Both constitutive and induced secondary metabolites are involved in plant defense against pathogens and chemical signals are also important in the establishment and maintenance of resource mutualisms. For example, both rhizobia and mycorrhizae depend on chemical signals, such as strigolactones and flavanoids exuded from plant roots, in order to find a suitable host.

For microbes to gain access to the plant, they must be able to penetrate the layer of wax that forms a hydrophobic barrier on the plant's surface. Many plant-pathogenic microbes secrete enzymes that break down these cuticular waxes. [7] Mutualistic microbes on the other hand may be granted access. For example, rhizobia secrete Nod factors that trigger the formation of an infection thread in receptive plants. The rhizobial symbionts can then travel through this infection thread to gain entrance to root cells.

Mycorrhizae and other fungal endophytes may also benefit their host plants by producing antibiotics or other secondary metabolites that ward off harmful fungi, bacteria and herbivores in the soil. [8] Some entomopathogenic fungi can also form endophytic relationships with plants and may even transfer nitrogen directly to plants from insects they consume in the surrounding soil. [9]

Plant-plant interactions

Allelopathy

Many plants produce secondary metabolites (known as allelochemicals) that can inhibit the growth of neighboring plants. Many examples of allelopathic competition have been controversial due to the difficulty of positively demonstrating a causal link between allelopathic substances and plant performance under natural conditions, [10] but it is widely accepted that phytochemicals are involved in competitive interactions between plants. One of the clearest examples of allelopathy is the production of juglone by walnut trees, whose strong competitive effects on neighboring plants were recognized in the ancient world as early as 36 BC. [11]

Plant-plant communication

Plants communicate with each other through both airborne and below-ground chemical cues. For example, when damaged by an herbivore, many plants emit an altered bouquet of volatile organic compounds (VOCs). Various C6 fatty acids and alcohols (sometimes known as green leaf volatiles) are often emitted from damaged leaves, since they are break-down products of plant cell membranes. These compounds (familiar to many as the smell of freshly mown grass) can be perceived by neighboring plants where they may trigger the induction of plant defenses. [12] It is debated to what extent this communication reflects a history of active selection due to mutual benefit as opposed to "eavesdropping" on cues unintentionally emitted by neighboring plants. [13]

Marine chemical ecology

Defense

Zoanthus sociatus produces palytoxin Vi - Zoanthus sociatus - 2.jpg
Zoanthus sociatus produces palytoxin

Many marine organisms use chemical defenses to deter predators. For example, some crustaceans and mesograzers, such as the Pseudamphithoides incurvaria , use toxic algae and seaweeds as a shield against predation by covering their bodies in these plants. These plants produce diterpenes such as pachydictyol-A and dictyol-E, which have been shown to deter predators.[ citation needed ] Other marine organisms produce chemicals endogenously to defend themselves. For example, the finless sole ( Pardachirus marmoratus ) produces a toxin that paralyzes the jaws of would-be predators. Many zoanthids produce potent toxins, such as palytoxin, which is one of the most poisonous known substances. Some species of these zooanthids are very brightly colored, which may be indicative of aposematic defense. [14]

Reproduction

Many marine organisms use pheromones to find mates. For example, male sea lampreys attract ovulating females by emitting a bile that can be detected many meters downstream. [15] Other processes can be more complex, such as the mating habits of crabs. Due to the fact that female crabs can only mate during a short period after moults from her shell, female crabs produces pheromones before she begins to moult in order to attract a mate. Male crabs will detect these pheromones and defend their potential mate until she has finished molted. However, due to the cannibalistic tendencies of crabs, the female produces an additional pheromone to suppresses cannibalistic instincts in her male guardian. These pheromones are very potent—so much so that they can induce male crabs to try to copulate with rocks or sponges that have been coated in pheromone by researchers. [16]

Dominance

American lobster (Homarus americanus) American lobster, Homarus americanus in Newfoundland, Canada (20996211958).jpg
American lobster ( Homarus americanus )

Dominance among crustaceans is also mediated through chemical cues. When crustaceans fight to determine dominance they urinate into the water. Later, if they meet again, both individuals can recognize each other by pheromones contained in their urine, allowing them to avoid a fight, if dominance has already been established. When a lobster encounters the urine of another individual, it will act differently according to the perceived status of the urinator (e.g. more submissively when exposed to the urine of a more dominant crab, or more boldly when exposed to the urine of a subdominant individual). When individuals are unable to communicate through urine, fights may be longer and more unpredictable. [16]

Applications of chemical ecology

Pheromone trap used to catch the pest Lymantria monacha. Feromon trap lymantria monacha 2 beentree.jpg
Pheromone trap used to catch the pest Lymantria monacha .

Pest Control

Chemical ecology has been utilized in the development of sustainable pest control strategies. Semiochemicals (especially insect sex pheromones) are widely used in integrated pest management for surveillance, trapping and mating disruption of pest insects. [17] Unlike conventional insecticides, pheromone-based methods of pest control are generally species-specific, non-toxic and extremely potent. In forestry, mass trapping has been used successfully to reduce tree mortality from bark beetle infestations in spruce and pine forests and from palm weevils in palm plantations. [17] In an aquatic system, a sex pheromone from the invasive sea lamprey has been registered by the United States Environmental Protection Agency for deployment in traps. [18] A strategy has been developed in Kenya to protect cattle from trypanosomiasis spread by Tsetse fly by applying a mixture of repellent odors derived from a non-host animal, the waterbuck. [19]

The successful push-pull agricultural pest management system makes use of chemical cues from intercropped plants to sustainably increase agricultural yields. The efficacy of push-pull agriculture relies on multiple forms of chemical communication. Though the push-pull technique was invented as a strategy to control stem-boring moths, such as Chilo partellus , through the manipulation of volatile host-finding cues, it was later discovered that allelopathic substances exuded by the roots of Desmodium spp. also contribute to the suppression of the damaging parasitic weed, Striga . [20]

Drug development and biochemistry discoveries

A large proportion of commercial drugs (e.g. aspirin, ivermectin, cyclosporin, taxol) are derived from natural products that evolved due to their involvement in ecological interactions. While it has been proposed that the study of natural history could contribute to the discovery of new drug leads, most drugs derived from natural products were not discovered due to prior knowledge of their ecological functions. [21] However, many fundamental biological discoveries have been facilitated by the study of plant toxins. For example, the characterization of the nicotinic acetylcholine receptor, the first neurotransmitter receptor to be identified, ensued from investigations into the mechanisms of action of curare and nicotine. Similarly, the muscarinic acetylcholine receptor takes its name from the fungal toxin muscarine. [22]

History of chemical ecology

After 1950

Silk moth (Bombyx mori) CSIRO ScienceImage 10746 An adult silkworm moth.jpg
Silk moth (Bombyx mori)

In 1959, Adolf Butenandt identified the first intraspecific chemical signal (bombykol) from the silk moth, Bombyx mori , with material obtained by grinding up 500,000 moths. [23] The same year, Karlson and Lüscher proposed the term 'pheromone' to describe this type of signal. [24] Also in 1959, Gottfried S. Fraenkel also published his landmark paper, "The Raison d'être of Secondary Plant Substances", arguing that plant secondary metabolites are not metabolic waste products, but actually evolved to protect plants from consumers. [25] Together, these papers marked the beginning of modern chemical ecology. In 1964, Paul R. Ehrlich and Peter H. Raven coauthored a paper proposing their influential theory of escape and radiate coevolution, which suggested that an evolutionary "arms-race" between plants and insects can explain the extreme diversification of plants and insects. [26] The idea that plant metabolites could not only contribute to the survival of individual plants, but could also influence broad macroevolutionary patterns, would turn out to be highly influential. However, Tibor Jermy questioned the view of an evolutionary arms race between plants and their insect herbivores and proposed that the evolution of phytophagous insects followed and follows that of plants without major evolutionary feedback, i.e. without affecting plant evolution. [27] He coined the term sequential evolution to describe plant-insect macroevolutionary patterns, which emphasizes that selection pressure exerted by insect attack on plants is weak or lacking. [28]

In the 1960s and 1970s, a number of plant biologists, ecologists, and entomologists expanded this line of research on the ecological roles of plant secondary metabolites. During this period, Thomas Eisner and his close collaborator Jerrold Meinwald published a series seminal papers on chemical defenses in plants and insects. [29] [30] A number of other scientists at Cornell were also working on topics related to chemical ecology during this period, including Paul Feeny, Wendell L. Roelofs, Robert Whittaker and Richard B. Root. In 1968, the first course in chemical ecology was initiated at Cornell. [31] In 1970, Eisner, Whittaker and the ant biologist William L. Brown, Jr. coined the terms allomone (to describe semiochemicals that benefit the emitter, but not the receiver) and kairomone (to describe semiochemicals that benefit the receiver only). [32] Whittaker and Feeny published an influential review paper in Science the following year, summarizing the recent research on the ecological roles of chemical defenses in a wide variety of plants and animals and likely introducing Whittaker's new taxonomy of semiochemicals to a broader scientific audience. [33] Around this time, Lincoln Brower also published a series of important ecological studies on monarch sequestration of cardenolides. Brower has been credited with popularizing the term "ecological chemistry" which appeared in the title of a paper he published in Science in 1968 [34] and again the following year in an article he wrote for Scientific American , where the term also appeared on the front cover under an image of a giant bluejay towering over two monarch butterflies. [24] [35]

The specialized Journal of Chemical Ecology was established in 1975, and the journal Chemoecology was founded in 1990. In 1984, the International Society of Chemical Ecology was established and in 1996, the Max Planck Institute of Chemical Ecology was founded in Jena, Germany. [24]

See also

Related Research Articles

<span class="mw-page-title-main">Pheromone</span> Secreted or excreted chemical factor that triggers a social response in members of the same species

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 like hormones outside the body of the secreting individual, to affect the behavior of the receiving individuals. There are alarm pheromones, food trail pheromones, sex pheromones, and many others that affect behavior or physiology. Pheromones are used by many organisms, from basic unicellular prokaryotes to complex multicellular eukaryotes. Their use among insects has been particularly well documented. In addition, some vertebrates, plants and ciliates communicate by using pheromones. The ecological functions and evolution of pheromones are a major topic of research in the field of chemical ecology.

<span class="mw-page-title-main">Allelopathy</span> Production of biochemicals which affect the growth of other organisms

Allelopathy is a biological phenomenon by which an organism produces one or more biochemicals that influence the germination, growth, survival, and reproduction of other organisms. These biochemicals are known as allelochemicals and can have beneficial or detrimental effects on the target organisms and the community. Allelopathy is often used narrowly to describe chemically-mediated competition between plants; however, it is sometimes defined more broadly as chemically-mediated competition between any type of organisms. Allelochemicals are a subset of secondary metabolites, which are not directly required for metabolism of the allelopathic organism.

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

Carminic acid (C22H20O13) is a red glucosidal hydroxyanthrapurin that occurs naturally in some scale insects, such as the cochineal, Armenian cochineal, and Polish cochineal. The insects produce the acid as a deterrent to predators. An aluminum salt of carminic acid is the coloring agent in carmine, a pigment. Natives of Peru had been producing cochineal dyes for textiles since at least 700 CE. Synonyms are C.I. 75470 and C.I. Natural Red 4.

Thomas Eisner was a German-American entomologist and ecologist, known as the "father of chemical ecology." He was a Jacob Gould Schurman Professor of Chemical Ecology at Cornell University, and Director of the Cornell Institute for Research in Chemical Ecology (CIRCE). He was a world authority on animal behavior, ecology, and evolution, and, together with his Cornell colleague Jerrold Meinwald, was one of the pioneers of chemical ecology, the discipline dealing with the chemical interactions of organisms. He was author or co-author of some 400 scientific articles and seven books.

<span class="mw-page-title-main">Allomone</span> Chemical communication between species that benefits the first but not the second

An allomone is a type of semiochemical produced and released by an individual of one species that affects the behaviour of a member of another species to the benefit of the originator but not the receiver. Production of allomones is a common form of defense against predators, particularly by plant species against insect herbivores. In addition to defense, allomones are also used by organisms to obtain their prey or to hinder any surrounding competitors.

A semiochemical, from the Greek σημεῖον (semeion), meaning "signal", is a chemical substance or mixture released by an organism that affects the behaviors of other individuals. Semiochemical communication can be divided into two broad classes: communication between individuals of the same species (intraspecific) or communication between different species (interspecific).

A kairomone is a semiochemical, emitted by an organism, which mediates interspecific interactions in a way that benefits an individual of another species which receives it and harms the emitter. This "eavesdropping" is often disadvantageous to the producer. The kairomone improves the fitness of the recipient and in this respect differs from an allomone and a synomone. The term is mostly used in the field of entomology. Two main ecological cues are provided by kairomones; they generally either indicate a food source for the receiver, or the presence of a predator, the latter of which is less common or at least less studied.

<span class="mw-page-title-main">Plant defense against herbivory</span> Plants defenses against being eaten

Plant defense against herbivory or host-plant resistance (HPR) is a range of adaptations evolved by plants which improve their survival and reproduction by reducing the impact of herbivores. Plants can sense being touched, and they can use several strategies to defend against damage caused by herbivores. Many plants produce secondary metabolites, known as allelochemicals, that influence the behavior, growth, or survival of herbivores. These chemical defenses can act as repellents or toxins to herbivores or reduce plant digestibility. Another defensive strategy of plants is changing their attractiveness. To prevent overconsumption by large herbivores, plants alter their appearance by changing their size or quality, reducing the rate at which they are consumed.

Sensory ecology is a relatively new field focusing on the information organisms obtain about their environment. It includes questions of what information is obtained, how it is obtained, and why the information is useful to the organism.

<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">John A. Pickett</span> British chemist (born 1945)

John Anthony Pickett CBE DSC FRS FLSW is a British chemist who is noted for his work on insect pheromones. Pickett is Professor of Biological Chemistry in the School of Chemistry at Cardiff University. He previously served as the Michael Elliott Distinguished Research Fellow at Rothamsted Research.

Pyrrolizidine alkaloid sequestration by insects is a strategy to facilitate defense and mating. Various species of insects have been known to use molecular compounds from plants for their own defense and even as their pheromones or precursors to their pheromones. A few Lepidoptera have been found to sequester chemicals from plants which they retain throughout their life and some members of Erebidae are examples of this phenomenon. Starting in the mid-twentieth century researchers investigated various members of Arctiidae, and how these insects sequester pyrrolizidine alkaloids (PAs) during their life stages, and use these chemicals as adults for pheromones or pheromone precursors. PAs are also used by members of the Arctiidae for defense against predators throughout the life of the insect.

Green leaf volatiles (GLV) are organic compounds released by plants. Some of these chemicals function as signaling compounds between either plants of the same species, of other species, or even different lifeforms like insects.

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

Chemical defense is a strategy employed by many organisms to avoid consumption by producing toxic or repellent metabolites or chemical warnings which incite defensive behavioral changes. The production of defensive chemicals occurs in plants, fungi, and bacteria, as well as invertebrate and vertebrate animals. The class of chemicals produced by organisms that are considered defensive may be considered in a strict sense to only apply to those aiding an organism in escaping herbivory or predation. However, the distinction between types of chemical interaction is subjective and defensive chemicals may also be considered to protect against reduced fitness by pests, parasites, and competitors. Repellent rather than toxic metabolites are allomones, a sub category signaling metabolites known as semiochemicals. Many chemicals used for defensive purposes are secondary metabolites derived from primary metabolites which serve a physiological purpose in the organism. Secondary metabolites produced by plants are consumed and sequestered by a variety of arthropods and, in turn, toxins found in some amphibians, snakes, and even birds can be traced back to arthropod prey. There are a variety of special cases for considering mammalian antipredatory adaptations as chemical defenses as well.

Insects have a wide variety of predators, including birds, reptiles, amphibians, mammals, carnivorous plants, and other arthropods. The great majority (80–99.99%) 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 ongoing escapist battle, insects have evolved a wide range of defense mechanisms. The only restraint on these adaptations is that their cost, in terms of time and energy, does not exceed the benefit that they provide to the organism. The further that a feature tips the balance towards beneficial, the more likely that selection will act upon the trait, passing it down to further generations. The opposite also holds true; defenses that are too costly will have a little chance of being passed down. Examples of defenses that have withstood the test of time include hiding, escape by flight or running, and firmly holding ground to fight as well as producing chemicals and social structures that help prevent predation.

Trail pheromones are semiochemicals secreted from the body of an individual to affect the behavior of another individual receiving it. Trail pheromones often serve as a multi purpose chemical secretion that leads members of its own species towards a food source, while representing a territorial mark in the form of an allomone to organisms outside of their species. Specifically, trail pheromones are often incorporated with secretions of more than one exocrine gland to produce a higher degree of specificity. Considered one of the primary chemical signaling methods in which many social insects depend on, trail pheromone deposition can be considered one of the main facets to explain the success of social insect communication today. Many species of ants, including those in the genus Crematogaster use trail pheromones.

<span class="mw-page-title-main">Tritrophic interactions in plant defense</span> Ecological interactions

Tritrophic interactions in plant defense against herbivory describe the ecological impacts of three trophic levels on each other: the plant, the herbivore, and its natural enemies. They may also be called multitrophic interactions when further trophic levels, such as soil microbes, endophytes, or hyperparasitoids are considered. Tritrophic interactions join pollination and seed dispersal as vital biological functions which plants perform via cooperation with animals.

<span class="mw-page-title-main">Jerrold Meinwald</span> American chemist and pharmacologist (1927–2018)

Jerrold Meinwald was an American chemist known for his work on chemical ecology, a field he co-founded with his colleague and friend Thomas Eisner. He was a Goldwin Smith Professor Emeritus of Chemistry at Cornell University. He was author or co-author of well over 400 scientific articles. His interest in chemistry was sparked by fireworks done with his friend Michael Cava when they were still in junior high school. Meinwald was also a music aficionado and studied flute with Marcel Moyse – the world's greatest flutist of his time.

A phytobiome consists of a plant (phyto) situated in its specific ecological area (biome), including its environment and the associated communities of organisms which inhabit it. These organisms include all macro- and micro-organisms living in, on, or around the plant including bacteria, archaea, fungi, protists, insects, animals, and other plants. The environment includes the soil, air, and climate. Examples of ecological areas are fields, rangelands, forests. Knowledge of the interactions within a phytobiome can be used to create tools for agriculture, crop management, increased health, preservation, productivity, and sustainability of cropping and forest systems.

<span class="mw-page-title-main">Chemical communication in insects</span>

Chemical communication in insects is social signalling between insects of the same or different species, using chemicals. These chemicals may be volatile, to be detected at a distance by other insects' sense of smell, or non-volatile, to be detected on an insect's cuticle by other insects' sense of taste. Many of these chemicals are pheromones, acting like hormones outside the body.

References

  1. ↑ "What is Chemical Ecology? | Chemical Ecology". NCBS. Retrieved 2017-12-10.
  2. 1 2 Dyer, Lee A.; Philbin, Casey S.; Ochsenrider, Kaitlin M.; Richards, Lora A.; Massad, Tara J.; Smilanich, Angela M.; Forister, Matthew L.; Parchman, Thomas L.; Galland, Lanie M. (2018-05-25). "Modern approaches to study plant–insect interactions in chemical ecology". Nature Reviews Chemistry. 2 (6): 50–64. doi:10.1038/s41570-018-0009-7. ISSN   2397-3358. S2CID   49362070.
  3. ↑ Wood William F. (1983). "Chemical Ecology: Chemical Communication in Nature". Journal of Chemical Education. 60 (7): 531–539. doi:10.1021/ed060p531.
  4. ↑ Meinwald, J.; Eisner, T. (19 March 2008). "Chemical ecology in retrospect and prospect". Proceedings of the National Academy of Sciences. 105 (12): 4539–4540. doi: 10.1073/pnas.0800649105 . ISSN   0027-8424. PMC   2290750 . PMID   18353981.
  5. 1 2 Mithfer, Axel; Boland, Wilhelm; Maffei, Massimo E. (2008), "Chemical Ecology of Plant–Insect Interactions", Molecular Aspects of Plant Disease Resistance, Wiley-Blackwell, pp. 261–291, doi:10.1002/9781444301441.ch9, ISBN   978-1-4443-0144-1
  6. ↑ Dyer, Lee A.; Philbin, Casey S.; Ochsenrider, Kaitlin M.; Richards, Lora A.; Massad, Tara J.; Smilanich, Angela M.; Forister, Matthew L.; Parchman, Thomas L.; Galland, Lanie M. (2018-05-25). "Modern approaches to study plant–insect interactions in chemical ecology". Nature Reviews Chemistry. 2 (6): 50–64. doi:10.1038/s41570-018-0009-7. ISSN   2397-3358. S2CID   49362070.
  7. ↑ Müller, Caroline; Riederer, Markus (2005). "Plant Surface Properties in Chemical Ecology". Journal of Chemical Ecology. 31 (11): 2621–2651. doi:10.1007/s10886-005-7617-7. ISSN   0098-0331. PMID   16273432. S2CID   33373155.
  8. ↑ Spiteller, Peter (2015). "Chemical ecology of fungi". Natural Product Reports. 32 (7): 971–993. doi:10.1039/C4NP00166D. PMID   26038303.
  9. ↑ Behie, S. W., P. M. Zelisko, and M. J. Bidochka. 2012. Endophytic Insect-Parasitic Fungi Translocate Nitrogen Directly from Insects to Plants. Science 336:1576–1577.
  10. ↑ Duke, S. O. 2010. Allelopathy: Current status of research and future of the discipline: A commentary.
  11. ↑ Willis, R. J. 2000. Juglans spp., juglone and allelopathy. Allelopathy Journal 7:1–55.
  12. ↑ Arimura, Gen-ichiro; Matsui, Kenji; Takabayashi, Junji (2009-05-01). "Chemical and Molecular Ecology of Herbivore-Induced Plant Volatiles: Proximate Factors and Their Ultimate Functions". Plant and Cell Physiology. 50 (5): 911–923. doi: 10.1093/pcp/pcp030 . ISSN   0032-0781. PMID   19246460 . Retrieved 2017-10-11.
  13. ↑ Heil, M., and R. Karban. 2010. Explaining evolution of plant communication by airborne signals. Trends in Ecology & Evolution 25:137–144.
  14. ↑ Bakus, Gerald J.; Targett, Nancy M.; Schulte, Bruce (1986). "Chemical ecology of marine organisms: An overview". Journal of Chemical Ecology. 12 (5): 951–987. doi:10.1007/bf01638991. ISSN   0098-0331. PMID   24307042. S2CID   34594704.
  15. ↑ Li, Weiming; Scott, Alexander P.; Siefkes, Michael J.; Yan, Honggao; Liu, Qin; Yun, Sang-Seon; Gage, Douglas A. (2002-04-05). "Bile Acid Secreted by Male Sea Lamprey That Acts as a Sex Pheromone". Science. 296 (5565): 138–141. Bibcode:2002Sci...296..138L. doi:10.1126/science.1067797. ISSN   0036-8075. PMID   11935026. S2CID   1688247 . Retrieved 2020-10-19.
  16. 1 2 Hay, Mark E. (2009). "Marine Chemical Ecology: Chemical Signals and Cues Structure Marine Populations, Communities, and Ecosystems". Annual Review of Marine Science. 1: 193–212. Bibcode:2009ARMS....1..193H. doi:10.1146/annurev.marine.010908.163708. ISSN   1941-1405. PMC   3380104 . PMID   21141035.
  17. 1 2 Witzgall, P., P. Kirsch, and A. Cork. 2010. Sex Pheromones and Their Impact on Pest Management. J Chem Ecol 36:80–100.
  18. ↑ KleinJan. 20, K., 2016, and 1:30 Pm. 2016. So long suckers! Sex pheromone may combat destructive lampreys.
  19. ↑ Saini, R. K., B. O. Orindi, N. Mbahin, J. A. Andoke, P. N. Muasa, D. M. Mbuvi, C. M. Muya, J. A. Pickett, and C. W. Borgemeister. 2017. Protecting cows in small holder farms in East Africa from tsetse flies by mimicking the odor profile of a non-host bovid. PLOS Neglected Tropical Diseases 11:e0005977. Public Library of Science.
  20. ↑ Khan, Z., C. Midega, J. Pittchar, J. Pickett, and T. Bruce. 2011. Push—pull technology: a conservation agriculture approach for integrated management of insect pests, weeds and soil health in Africa. International Journal of Agricultural Sustainability 9:162–170. Taylor & Francis.
  21. ↑ Caporale, L. H. 1995. Chemical ecology: a view from the pharmaceutical industry. Proceedings of the National Academy of Sciences 92:75–82.
  22. ↑ Martindale, R., and R. A. J. Lester. 2014. On the Discovery of the Nicotinic Acetylcholine Receptor Channel. Pp. 1–16 in R. A. J. Lester, ed. Nicotinic Receptors. Springer, New York, NY.
  23. ↑ Wyatt, T. D. 2009. Fifty years of pheromones. Nature 457:262–263. Nature Publishing Group.
  24. 1 2 3 Bergström, G. 2007. Chemical ecology = chemistry + ecology! Pure and Applied Chemistry 79:2305–2323.
  25. ↑ Fraenkel, G. S. 1959. The Raison d’Être of Secondary Plant Substances: These odd chemicals arose as a means of protecting plants from insects and now guide insects to food. Science 129:1466–1470. American Association for the Advancement of Science.
  26. ↑ Ehrlich, P. R., and P. H. Raven. 1964. Butterflies and Plants: A Study in Coevolution. Evolution 18:586–608.
  27. ↑ Jermy, Tibor (1984). "Evolution of insect/host plant relationships". The American Naturalist. 124 (5): 609–630.
  28. ↑ Jermy, Tibor (1993). "Evolution of insect-plant relationships - a devil's advocate approach". Entomologia Experimentalis et Applicata. 66 (1): 3–12.
  29. ↑ Eisner, T. (4 December 1964). "Catnip: Its Raison d'Etre". Science. 146 (3649): 1318–1320. Bibcode:1964Sci...146.1318E. doi:10.1126/science.146.3649.1318. ISSN   0036-8075. PMID   14207462. S2CID   11282193.
  30. ↑ Eisner, Thomas; Meinwald, Jerrold (1966). "Defensive Secretions of Arthropods". Science. 153 (3742): 1341–1350. Bibcode:1966Sci...153.1341E. doi:10.1126/science.153.3742.1341. ISSN   0036-8075. JSTOR   1719969. PMID   17814381 . Retrieved 2020-10-25.
  31. ↑ "History and Introduction".
  32. ↑ Brown, W. L., T. Eisner, and R. H. Whittaker. 1970. Allomones and Kairomones: Transspecific Chemical Messengers. BioScience 20:21–21. Oxford Academic.
  33. ↑ Whittaker, R. H., and P. P. Feeny. 1971. Allelochemics: Chemical Interactions between Species. Science 171:757–770. American Association for the Advancement of Science.
  34. ↑ Brower, L. P., W. N. Ryerson, L. L. Coppinger, and S. C. Glazier. 1968. Ecological Chemistry and the Palatability Spectrum. Science 161:1349–1350. American Association for the Advancement of Science.
  35. ↑ "Dr. Lincoln Brower". 3 August 2018.

Further reading

This page is based on this Wikipedia article
Text is available under the CC BY-SA 4.0 license; additional terms may apply.
Images, videos and audio are available under their respective licenses.