Mycangium

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Pronotal mycangia of ambrosia beetle Xylosandrus crassiusculus Pronotal mycangium from ambrosia beetle.jpg
Pronotal mycangia of ambrosia beetle Xylosandrus
crassiusculus

The term mycangium (pl., mycangia) is used in biology for special structures on the body of an animal that are adapted for the transport of symbiotic fungi (usually in spore form). This is seen in many xylophagous insects (e.g. horntails and bark beetles), which apparently derive much of their nutrition from the digestion of various fungi that are growing amidst the wood fibers. In some cases, as in ambrosia beetles (Coleoptera: Curculionidae: Scolytinae and Platypodinae), the fungi are the sole food, and the excavations in the wood are simply to make a suitable microenvironment for the fungus to grow. In other cases (e.g., the southern pine beetle, Dendroctonus frontalis ), wood tissue is the main food, and fungi weaken the defense response from the host plant. [1]

Contents

Some species of phoretic mites that ride on the beetles, have their own type of mycangium, but for historical reasons, mite taxonomists use the term acarinarium. Apart from riding on the beetles, the mites live together with them in their burrows in the wood. [2] [3]

Origin

These structures were first systematically described by Helene Francke-Grosmann at 1956. [4] Then Lekh R. Batra [5] coined the word mycangia: [6] modern Latin, from Greek myco 'fungus' + angeion 'vessel'.

Function

The most common function of mycangia is preserving and releasing symbiotic inoculum. Usually, the symbiotic inoculum in mycangia will benefit their vectors (typically insect or mites), helping them to adapt to the new environment or provide nutrients of the vectors themselves and their descendants. [7]

For example, the ambrosia beetle ( Euwallacea fornicatus ) carries the symbiotic fungus Fusarium . When the beetle bores a host plant, it releases the symbiotic fungus from its mycangium. The symbiotic fungus becomes a plant pathogen, acting to weaken the resistance of host plant. [8] In the meantime, the fungus grows quickly in the galleries as the main food of beetle. [8] After reproduction, maturing beetles will fill their mycangia with symbiont before hunting for a new host plant. [9]

Therefore, mycangia play an important role in protecting the inoculum from degradation and contamination. The structures of mycangia always resemble a pouch or a container, with caps or a small opening that reduce the possibility of contaminants from outside. [4] How mycangia release their inoculum is still unknown.

Mycangia and symbiotic inoculum

Most of the inoculum in mycangia are fungi. The symbiotic inoculum of most bark and ambrosia beetles are fungi belonging to Ophiostomatales (Ascomycota: Sordariomycetidae) and Microascales (Ascomycota: Hypocreomycetidae). [7] Symbiotic fungi in mycangia of woodwasps are Amylostereaceae (Basidiomycota: Russulales). [10] Symbiotic fungi in mycangia of lizard beetles are yeast (Ascomycota: Saccharomycetales). [11] Symbiotic fungi in mycangia of ship-timber beetles are Endomyces (Ascomycota: Dipodascaceae). [12] Symbiotic fungi in mycangia of leaf-rolling weevils are Penicillium fungi (Ascomycota: Trichocomaceae). [13] In addition to the above primary symbiotic fungi, secondary fungi and some bacteria have been isolated from mycangia. [14]

Mycangia in insects

Mycangia in bark and ambrosia beetles

Oral mycangia in ambrosia beetle Ambrosiodmus Oral mycangia.gif
Oral mycangia in ambrosia beetle Ambrosiodmus

Mycangia of bark and ambrosia beetles (Curculionidae: Scolytinae and Platypodinae) are often complex cuticular invaginations for transport of symbiotic fungi. [2] [7] Phloem-feeding bark beetles (Curculionidae: Scolytinae) have usually numerous small pits on the surface of their body, while ambrosia beetles (many Scolytinae and all Platypodinae), which are completely dependent on their fungal symbiont, have deep and complicated pouches. [7] These mycangia are often equipped with glands secreting substances to support fungal spores and perhaps to nourish mycelium during transport. [15] In many cases, the entrance to a mycangium is surrounded by tufts of setae, aiding in scraping mycelium and spores from walls of the tunnels and directing the spores into the mycangium. The mycangia of ambrosia beetle are highly diverse. Different genera or tribes with different kinds of mycangia. Some are oral mycangia in the head, [7] such as genus Ambrosiodmus and Euwallacea . [16] Some are pronotal mycangia, such genus Xylosandrus and Cnestus. [17]

Mycangia in woodwasps (horntails)

Mycangia of the woodwasps (Hymenoptera: Siricidae) were first described by Buchner. [18] Different from highly diverse types in bark and ambrosia beetles, woodwasps only have a pair of mycangia on the top of their ovipositor. Then when females deposit their eggs inside the host plant, they inject the symbiotic fungi from mycangia and phytotoxic mucus from another reservoir-like structure. [19]

Mycangia in lizard beetles

One species of lizard beetle Doubledaya bucculenta (Coleoptera: Erotylidae: Erotylidae) has mycangia on the tergum of the eighth abdominal segment. This ovipositor-associated mycangia is only present in adult females. Before Doubledaya bucculentnta deposit their eggs and inject the symbiotic microorganisms on a recently dead bamboo, they will excavate a small hole through the bamboo culm. [11]

Mycangia in ship-timber beetles

The ship-timber beetle (Coleoptera: Lymexylidae) is another family of wood-boring beetles that live with symbiotic fungi. Buchner first discovered their mycangia located on the ventral side of the long ovipositor. [20] These mycangia form a pair of integumental pouches at either side near the tip of oviduct. When the female lays the eggs, new eggs are coated with the fungal spores.

Mycangia in leaf-rolling weevils

Females of the leaf-rolling weevil in the genus Euops (Coleoptera: Attelabidae) store symbiotic fungi in the mycangia, which is between the first ventral segment of the abdomen and the thorax. [13] Different from ovipositor-associate mycangia in woodwasps, lizard beetles, and ship-timber beetles, mycangia of leaf-rolling weevils is a pair of spore incubators at the anterior end of the abdomen. This mycangium is formed by the coxa and the metendosternite at the posterior end of the thorax. [10]

Mycangia in stag beetles

Lesser stag beetle female everting the mycangium soon after eclosion Dorcus parallelipipedus female mycangium.jpg
Lesser stag beetle female everting the mycangium soon after eclosion

Mycangia of the stag beetles (Coleoptera: Lucanidae) were discovered in Japan only this century. [21] This ovipositor-associated mycangium is located in a dorsal fold of the integument between the last two tergal plates of the adult females. It has been examined in many species. [22] [23] [24] A female everts the mycangium for the first time soon after eclosion; this is to retrieve the symbionts left by the larva on the pupal chamber when it emptied its gut before pupating. Later, when ovipositing, she everts it to pass on the inoculum to the next generation. [25]

Related Research Articles

<span class="mw-page-title-main">Ascomycota</span> Division or phylum of fungi

Ascomycota is a phylum of the kingdom Fungi that, together with the Basidiomycota, forms the subkingdom Dikarya. Its members are commonly known as the sac fungi or ascomycetes. It is the largest phylum of Fungi, with over 64,000 species. The defining feature of this fungal group is the "ascus", a microscopic sexual structure in which nonmotile spores, called ascospores, are formed. However, some species of the Ascomycota are asexual, meaning that they do not have a sexual cycle and thus do not form asci or ascospores. Familiar examples of sac fungi include morels, truffles, brewers' and bakers' yeast, dead man's fingers, and cup fungi. The fungal symbionts in the majority of lichens such as Cladonia belong to the Ascomycota.

<span class="mw-page-title-main">Curculionidae</span> Family of beetles

The Curculionidae are a family of weevils, commonly called snout beetles or true weevils. They are one of the largest animal families with 6,800 genera and 83,000 species described worldwide. They are the sister group to the family Brentidae.

Ambrosia beetles are beetles of the weevil subfamilies Scolytinae and Platypodinae, which live in nutritional symbiosis with ambrosia fungi. The beetles excavate tunnels in dead, stressed, and healthy trees in which they cultivate fungal gardens, their sole source of nutrition. After landing on a suitable tree, an ambrosia beetle excavates a tunnel in which it releases spores of its fungal symbiont. The fungus penetrates the plant's xylem tissue, extracts nutrients from it, and concentrates the nutrients on and near the surface of the beetle gallery. Ambrosia fungi are typically poor wood degraders, and instead utilize less demanding nutrients. Symbiotic fungi produce and detoxify ethanol, which is an attractant for Ambrosia beetles and likely prevents growth of antagonistic pathogens and selects for other beneficial symbionts. The majority of ambrosia beetles colonize xylem of recently dead trees, but some attack stressed trees that are still alive, and a few species attack healthy trees. Species differ in their preference for different parts of trees, different stages of deterioration, and in the shape of their tunnels ("galleries"). However, the majority of ambrosia beetles are not specialized to any taxonomic group of hosts, unlike most phytophagous organisms including the closely related bark beetles. One species of ambrosia beetle, Austroplatypus incompertus exhibits eusociality, one of the few organisms outside of Hymenoptera and Isoptera to do so.

<span class="mw-page-title-main">Bark beetle</span> Subfamily of beetles

A bark beetle is the common name for the subfamily of beetles Scolytinae. Previously, this was considered a distinct family (Scolytidae), but is now understood to be a specialized clade of the "true weevil" family (Curculionidae). Although the term "bark beetle" refers to the fact that many species feed in the inner bark (phloem) layer of trees, the subfamily also has many species with other lifestyles, including some that bore into wood, feed in fruit and seeds, or tunnel into herbaceous plants. Well-known species are members of the type genus Scolytus, namely the European elm bark beetle S. multistriatus and the large elm bark beetle S. scolytus, which like the American elm bark beetle Hylurgopinus rufipes, transmit Dutch elm disease fungi (Ophiostoma). The mountain pine beetle Dendroctonus ponderosae, southern pine beetle Dendroctonus frontalis, and their near relatives are major pests of conifer forests in North America. A similarly aggressive species in Europe is the spruce ips Ips typographus. A tiny bark beetle, the coffee berry borer, Hypothenemus hampei is a major pest on coffee plantations around the world.

<span class="mw-page-title-main">Entomopathogenic fungus</span> Fungus that can act as a parasite of insects

An entomopathogenic fungus is a fungus that can kill or seriously disable insects.

<span class="mw-page-title-main">Fungivore</span> Organism that consumes fungi

Fungivory or mycophagy is the process of organisms consuming fungi. Many different organisms have been recorded to gain their energy from consuming fungi, including birds, mammals, insects, plants, amoebas, gastropods, nematodes, bacteria and other fungi. Some of these, which only eat fungi, are called fungivores whereas others eat fungi as only part of their diet, being omnivores.

<i>Xyleborus glabratus</i> Species of beetle

Xyleborus glabratus, the redbay ambrosia beetle, is a type of ambrosia beetle invasive in the United States. It has been documented as the primary vector of Raffaelea lauricola, the fungus that causes laurel wilt, a disease that can kill several North American tree species in the family Lauraceae, including redbay, sassafras, and avocado.

<i>Euops</i> Genus of beetles

Euops is a genus of the leaf-rolling weevils containing more than 300 species. It is spread over most tropical and subtropical regions but is missing from America. The centre of its radiation is New Guinea and Australia where it is the only representative of the subfamily Attelabinae.

<i>Austroplatypus incompertus</i> Species of beetle

Austroplatypus incompertus is a species of ambrosia beetle belonging to the true weevil family, native to Australia, with a verified distribution in New South Wales and Victoria. It forms colonies in the heartwood of Eucalyptus trees and is the first beetle to be recognized as a eusocial insect. Austroplatypus incompertus is considered eusocial because groups contain a single fertilized female that is protected and taken care of by a small number of unfertilized females that also do much of the work. The species likely passed on cultivated fungi to other weevils.

<span class="mw-page-title-main">European spruce bark beetle</span> Species of beetle

The European spruce bark beetle, is a species of beetle in the weevil subfamily Scolytinae, the bark beetles, and is found from Europe to Asia Minor and some parts of Africa.

<i>Euwallacea fornicatus</i> Species of beetle

Euwallacea fornicatus is a species complex consisting of multiple cryptic species of ambrosia beetles, known as an invasive species in California, Israel and South Africa. The species has also been unintentionally introduced into exotic greenhouses in several European countries. As the rest of the ambrosia beetles, E. fornicatus larvae and adults feed on a symbiotic fungus carried in a specific structure called mycangium. In E. fornicatus, the mycangium is located in the mandible. The combination of massive numbers of beetles with the symbiotic fungus kills trees, even though the fungus alone is a weak pathogen.

<i>Platypus cylindrus</i> Species of beetle

Platypus cylindrus, commonly known as the oak pinhole borer, is a species of ambrosia beetle in the weevil family Scolytinae. The adults and larvae burrow under the bark of mature oak trees. It is native to Europe.

<i>Xylosandrus germanus</i> Species of beetle

Xylosandrus germanus, known generally as the alnus ambrosia beetle or black stem borer, is a species of ambrosia beetle in the family Curculionidae. The black stem borer is native to eastern Asia, but is an invasive species in Europe and North America. It carries an associated ambrosia fungus, Ambrosiella grosmanniae.

Platypus quercivorus, the oak ambrosia beetle, is a species of weevil and pest of broad-leaved trees. This species is most commonly known for vectoring the fungus responsible for excessive oak dieback in Japan since the 1980s. It is found in Japan, India, Indonesia, New Guinea, and Taiwan.

Euplatypus parallelus, previously known as Platypus parallelus, is a species of ambrosia beetle in the weevil family Curculionidae. The adults and larvae form galleries in various species of tree and logs. It is native to Central and South America but has spread globally, is present in Africa and is well established in tropical Asia.

<i>Cnestus mutilatus</i> Species of beetle

Cnestus mutilatus, commonly known as the camphor shot borer, camphor shoot borer, or sweetgum ambrosia beetle, is a species of ambrosia beetle in the subfamily Scolytinae of the weevil family Curculionidae. It is native to Asia, but has been established as an invasive species in the United States since 1999.

Fungus pockets are any of various convergently evolved inoculum-retention and -cultivation organs in a wide range of insect taxa. They are generally divided into mycangia and infrabuccal pockets.

Euwallacea interjectus, is a species of weevil native to Asia but introduced to Westerns parts of the world.

Euwallacea piceus, is a species of weevil native to Oriental Asia but introduced to African and other Westerns Pacific parts of the world. It is a serious pest in tropical and subtropical parts of the Americas.

Euwallacea perbrevis, commonly known as tea shot-hole borer, is a species of weevil native to South and South-East Asia through to Australia, but introduced to Western countries.

References

  1. ↑ Paine, T. D.; Stephen, F. M. (1987-01-01). "Fungi Associated with the Southern Pine Beetle: Avoidance of Induced Defense Response in Loblolly Pine". Oecologia. 74 (3): 377–379. Bibcode:1987Oecol..74..377P. doi:10.1007/bf00378933. JSTOR   4218483. PMID   28312476. S2CID   20763037.
  2. 1 2 Francke-Grossmann H. (1967). Ectosymbiosis in wood inhabiting insects. In: M. Henry (ed.) Symbiosis, Vol. 2. Academic Press, New York. pp.141-205.
  3. ↑ Mori, Boyd A.; Proctor, Heather C.; Walter, David E.; Evenden, Maya L. (2011-02-01). "Phoretic mite associates of mountain pine beetle at the leading edge of an infestation in northwestern Alberta, Canada". The Canadian Entomologist. 143 (1): 44–55. doi:10.4039/n10-043. ISSN   1918-3240. S2CID   86284129.
  4. 1 2 Francke-Grosmann, H. 1956. Hautdrüsen als träger der pilzsymbiose bei ambrosiakäfern. Zeitschrift für Morphologie und Ökologie der Tiere 45: 275–308.
  5. ↑ Batra, Lekh (1963). "Ecology of ambrosia fungi and their dissemination by beetles". Transactions of the Kansas Academy of Science. 66 (2): 213–236. doi:10.2307/3626562. JSTOR   3626562.
  6. ↑ Batra, L. R. (1963). "Ecology of ambrosia fungi and their dissemination by beetles". Trans. Kans. Acad. Sci. 66 (2): 213–236. doi:10.2307/3626562. JSTOR   3626562.
  7. 1 2 3 4 5 Hulcr, Jiri; Stelinski, Lukasz L. (2017-01-31). "The Ambrosia Symbiosis: From Evolutionary Ecology to Practical Management". Annual Review of Entomology. 62 (1): 285–303. doi:10.1146/annurev-ento-031616-035105. PMID   27860522.
  8. 1 2 Kasson, Matthew T.; O'Donnell, Kerry; Rooney, Alejandro P.; Sink, Stacy; Ploetz, Randy C.; Ploetz, Jill N.; Konkol, Joshua L.; Carrillo, Daniel; Freeman, Stanley (2013-07-01). "An inordinate fondness for Fusarium: Phylogenetic diversity of fusaria cultivated by ambrosia beetles in the genus Euwallacea on avocado and other plant hosts". Fungal Genetics and Biology. 56: 147–157. doi:10.1016/j.fgb.2013.04.004. PMID   23608321.
  9. ↑ "tea shot-hole borer, Euwallacea fornicatus". Featured Creatures.
  10. 1 2 Sakurai, Kazuhiko (1985). "An attelabid weevil (Euops splendida) cultivates fungi". Journal of Ethology. 3 (2): 151–156. doi:10.1007/BF02350306. ISSN   0289-0771. S2CID   30261494.
  11. 1 2 Toki, Wataru; Tanahashi, Masahiko; Togashi, Katsumi; Fukatsu, Takema (2012-07-27). "Fungal Farming in a Non-Social Beetle". PLOS ONE. 7 (7): e41893. Bibcode:2012PLoSO...741893T. doi: 10.1371/journal.pone.0041893 . ISSN   1932-6203. PMC   3407107 . PMID   22848648.
  12. ↑ Lyngnes, A. R. (1958). "Studier over Hylecoetus dermestoides L. under et angrep på bjorkestokker på Sunnmore 1954-1955". Norsk Entomologisk Tidsskrif. 10: 221–235.
  13. 1 2 Kobayashi, Chisato; Fukasawa, Yu; Hirose, Dai; Kato, Makoto (2007-08-16). "Contribution of symbiotic mycangial fungi to larval nutrition of a leaf-rolling weevil". Evolutionary Ecology. 22 (6): 711–722. doi:10.1007/s10682-007-9196-2. ISSN   0269-7653. S2CID   29669166.
  14. ↑ Hulcr, J.; Rountree, N. R.; Diamond, S. E.; Stelinski, L. L.; Fierer, N.; Dunn, R. R. (2012-05-01). "Mycangia of Ambrosia Beetles Host Communities of Bacteria". Microbial Ecology. 64 (3): 784–793. doi: 10.1007/s00248-012-0055-5 . ISSN   0095-3628. PMID   22546962.
  15. ↑ Six, Diana (2003). "Bark beetle-fungus symbioses". Insect Symbiosis. Contemporary Topics in Entomology. 20032558: 97–144. doi:10.1201/9780203009918.ch7. ISBN   978-0-8493-1286-1.
  16. ↑ Li, You; Simmons, David Rabern; Bateman, Craig C.; Short, Dylan P. G.; Kasson, Matthew T.; Rabaglia, Robert J.; Hulcr, Jiri (2015-09-14). "New Fungus-Insect Symbiosis: Culturing, Molecular, and Histological Methods Determine Saprophytic Polyporales Mutualists of Ambrosiodmus Ambrosia Beetles". PLOS ONE. 10 (9): e0137689. Bibcode:2015PLoSO..1037689Y. doi: 10.1371/journal.pone.0137689 . ISSN   1932-6203. PMC   4569427 . PMID   26367271.
  17. ↑ Stone, W.D.; Nebeker, T.E.; Monroe, W.A.; MacGown, J.A. (2007-02-01). "Ultrastructure of the mesonotal mycangium of Xylosandrus mutilatus (Coleoptera: Curculionidae)". Canadian Journal of Zoology. 85 (2): 232–238. doi:10.1139/z06-205. ISSN   0008-4301.
  18. ↑ Buchner, P. 1928: Holznahrung und Symbiose. Vortrag gehalten auf dem X internationalen Zoologentag zu Budapest am 8. September 1927. Berlin: Springer, pp. 13–16.
  19. ↑ Coutts, M. P. (1969). "The mechanism of pathogenicity of Sirex noctilio in Pinus radiata. II. Effects of S. noctilio mucus". Aust. J. Biol. Sci. 22: 1153–1161. doi: 10.1071/BI9691153 .
  20. ↑ Casari, Sônia A.; Teixeira, Édson Possidônio (2011). "Larva of Atractocerus brasiliensis (Lepeletier & Audinet-Serville, 1825) (Lymexylidae, Atractocerinae)". Papéis Avulsos de Zoologia. 51 (12): 197–205. doi: 10.1590/S0031-10492011001200001 . ISSN   0031-1049.
  21. ↑ Tanahashi, M.; Kubota, K.; Matsushita, N.; Togashi, K. (2010). "Discovery of mycangia and the associated xylose-fermenting yeasts in stag beetles (Coleoptera: Lucanidae)". Naturwissenschaften. 97 (3): 311–317. Bibcode:2010NW.....97..311T. doi:10.1007/s00114-009-0643-5. PMID   20107974. S2CID   2650646.
  22. ↑ Tanahashi, M.; Kubota, K.; Matsushita, N.; Togashi, K. (2010). "Discovery of mycangia and the associated xylose-fermenting yeasts in stag beetles (Coleoptera: Lucanidae)". Naturwissenschaften. 97 (3): 311–317. Bibcode:2010NW.....97..311T. doi:10.1007/s00114-009-0643-5. PMID   20107974. S2CID   2650646.
  23. ↑ Tanahashi M., Fremlin M. (2013). "The mystery of the lesser stag beetle Dorcus parallelipipedus (L.) (Coleoptera: Lucanidae) mycangium yeasts". Bulletin of the Amateur Entomologists' Society. 72 (510): 146–152.
  24. ↑ Tanahashi, Masahiko; Hawes, Colin J. (2016). "The presence of a mycangium in European Sinodendron cylindricum(Coleoptera: Lucanidae) and the associated yeast symbionts". Journal of Insect Science. 16: 76. doi:10.1093/jisesa/iew054. PMC   4948600 . PMID   27432353.
  25. ↑ Fremlin M.; Tanahashi M. (2015). "Sexually-dimorphic post-eclosion behaviour in the European stag beetle Lucanus cervus (L.) (Coleoptera: Lucanidae)". Mitteilungen der Schweizerischen Entomologischen Gesellschaft. 88: 29–38.
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