Symbiotic fungi transform terpenes from spruce resin into attractants for bark beetles
When metabolizing spruce bark, the insect’s fungal partners release volatile compounds that bark beetles recognize through specialized olfactory sensory neurons
Peer-Reviewed PublicationIMAGE: EUROPEAN SPRUCE BARK BEETLE IPS TYPOGRAPHUS: THE NEWLY HATCHED YOUNG ADULT IS STILL IN THE SO-CALLED PUPAL CHAMBER AT THE END OF THE TUNNEL IT CREATED AS A LARVA. IT IS SURROUNDED BY SPORES OF A SYMBIOTIC FUNGUS. view more
CREDIT: DINESHKUMAR KANDASAMY AND VEIT GRABE, MAX PLANCK INSTITUTE FOR CHEMICAL ECOLOGY
The mass outbreaks of bark beetles observed in recent years have caused shocking amounts of forest damage throughout Germany. As reported by the Federal Statistical Office in July 2022, more than 80% of the trees that had to be felled in the previous year were damaged by insects. The damaged timber felled due to insect damage amounted to more than 40 million cubic meters. One of the main pests is the European spruce beetle Ips typographus. In the Thuringian Forest and the Harz Mountains, for example, the beetle, which is only a few millimeters long, encountered spruce monocultures that had already been weakened by high temperatures and extended periods of drought, which facilitated the spread of the pest and led to the death of huge forest stands within a short period of time.
Researchers have already known that chemical communication plays an important role in bark beetle mass attacks. Beetles first choose a suitable tree and then emit so-called aggregation pheromones. These pheromones attract conspecifics in the vicinity to join a mass attack that overcomes the tree’s defenses. Spruce trees whose defenses are already weakened by stresses are more readily overcome.
Bark beetles like the odor of their symbiotic fungi
Spruce bark beetles need fungal allies to successfully reproduce in the trees. The fungi are ectosymbionts, symbiotic partners that live outside the beetles. Each new generation of beetles must find their symbiotic fungi and carry them to a new host tree.
In a new study, an international research team led by Dineshkumar Kandasamy (now at Lund University, Sweden) and Jonathan Gershenzon of the Max Planck Institute for Chemical Ecology in Jena, Germany, reports that the European spruce bark beetle can find its fungal partners based on the volatile chemical compounds the fungi release when they degrade spruce resin components. “We had already been able to show that bark beetles are attracted to their fungal associates when these are cultured on standard fungal growth medium. Now we wanted to know what would happen if we grew fungi on a more natural medium with spruce bark powder added. Would beetles be attracted to fungi now? If so, which chemical compounds would be responsible for the attraction and what is the origin of these chemicals?” says first author Dineshkumar Kandasamy, explaining the study's initial questions.
Fungi convert the chemical defenses of spruce into attractants for the beetles
European spruce bark beetles are associated with fungal partners of different genera. The fungus Grosmannia penicillata grew particularly well on the spruce bark medium and produced more volatile compounds than most of the other fungi tested. Therefore the researchers focused their investigations on this fungus. The researchers set up special experimental arenas where they could test whether the beetles were attracted to volatile compounds emitted by the fungi.
“We first found that European spruce bark beetles are attracted to the volatiles emitted by their associated fungi when fungi were growing on medium with spruce bark powder. However, we also showed that fungi can transform terpene compounds from spruce resin into their oxygenated derivatives and that some of these metabolites produced by fungi are particularly attractive to bark beetles. The overall conclusion is that these volatiles serve as chemical signals that keep the symbiosis between bark beetles and their associated fungi going," says Dineshkumar Kandasamy.
The researchers found that pathogenic fungi, which are harmful to the beetles, can also metabolize spruce resin compounds. However, unlike the metabolites of the symbiotic fungi, the resulting derivatives are not attractive to bark beetles. Bark beetles can therefore use their sense of smell to distinguish whether the fungi present in the tree are good or bad for them. The scientists were particularly surprised when the behavioral observations revealed that fungal partners not only attracted the beetles but also stimulated them to tunnel.
Bark beetles have olfactory sensory cells in their antennae tuned to detect volatile compounds of fungal metabolism
Further evidence that fungal metabolites make spruce trees already infested by fungi even more attractive to bark beetles was provided by electrophysiological studies of the beetles' perception of these odors. This involved testing the response of individual olfactory sensilla on the beetle antennae to different odors. The researchers were able to show that the bark beetles possess certain olfactory sensory neurons housed in sensilla that are specialized in detecting oxygenated monoterpenes emitted by the fungi.
“By enhancing bark beetle attraction to particular trees, volatiles from the fungus could increase the intensity and success of mass attacks. Fungi may help kill the host tree, overcome its defenses, provide beetles with nutrients or protect them from pathogens. The ability of the fungus to metabolize resin components that are originally produced by the tree as a defense could indicate which fungi are virulent and could serve as good partners for the beetle," says Jonathan Gershenzon.
The results of this new study may help improve the control of bark beetle outbreaks. One of the most widely used strategy in the fight against these pests are pheromone traps, but these have not been effective in preventing recent outbreaks. Therefore, the researchers are now testing whether these odor traps can be optimized by adding oxygenated monoterpenes from fungal metabolism. An important goal for the research team is to learn more about the metabolism of the spruce resin compounds in the fungi and to find out whether this can be a detoxification reaction for the fungus or for the beetle.
Dineshkumar Kandasamy is currently supported by the Max Planck Center next Generation Insect Chemical Ecology research network, a Max Planck Society-funded collaboration of the Max Planck Institute for Chemical Ecology with Lund University and the Swedish University of Agricultural Sciences. The Max Planck Center aims to study the impact of anthropogenic global warming and air pollution on insect chemical communication. The focus is not only on pests, but also on pollinators and their ecosystem services, as well as insects that carry and transmit pathogens.
JOURNAL
PLoS Biology
METHOD OF RESEARCH
Experimental study
SUBJECT OF RESEARCH
Animals
ARTICLE TITLE
Conifer-killing bark beetles locate fungal symbionts by detecting volatile fungal metabolites of host tree resin monoterpenes
Conifer-killing beetles use smell of
beneficial fungus to select host trees
Bark beetles use specialized neurons to sense tree-resin derived compounds produced by the fungus
Peer-Reviewed PublicationIMAGE: PUPAE OF THE EUROPEAN SPRUCE BARK BEETLE (IPS TYPOGRAPHUS) IN THE BARK OF A NORWAY SPRUCE TREE (PICEA ABIES) RECENTLY KILLED BY BARK BEETLE ATTACK. view more
CREDIT: DINESHKUMAR KANDASAMY (CC BY 4.0, HTTPS://CREATIVECOMMONS.ORG/LICENSES/BY/4.0/)
Eurasian spruce bark beetles (Ips typographus) burrow into the bark of Norway spruce (Picea abies) trees where they mate and lay their eggs. Major outbreaks in Europe have decimated millions of hectares of conifer forests. The beetles preferentially attack trees that are already infected with symbiotic fungi (such as Grosmannia penicillata), which is thought to weaken host trees and break down their chemical defenses, allowing the beetles to successfully develop in the bark.
To investigate the chemical signals that the beetles use to identify host trees infected with the fungus, the researchers performed a series of laboratory experiments on captive bark beetles and samples of Norway spruce bark. They found that the fungus breaks down chemicals in tree bark resin, known as monoterpenes, into new compounds, including camphor and thujanol. After 12 days of infection, these fungus-produced compounds dominated the chemical mixture emitted by bark samples. Single cell recordings of sensory neurons in the beetles’ antennae showed that they can detect camphor and thujanol, and in behavioral experiments, bark beetles were attracted to bark containing the fungus-produced compounds.
Tree-resin derived compounds produced by the fungus may allow bark beetles to assess the presence of their symbiont, helping them to identify suitable sites for feeding and breeding. The authors say that understanding the role of these compounds in bark beetle attacks could be useful for pest-management strategies to protect European conifers from epidemic outbreaks.
Gershenzon adds, “The bark beetles currently killing millions of spruce trees every year in Europe are supported in their attacks by fungal associates. We discovered that these fungi convert volatile compounds from spruce resin to products, which may serve as cues for bark beetles to find them.”
Spore stalks and mycelia of Endoconidiophora polonica, a fungal symbiont of the European spruce bark beetle (Ips typographus) that is closely associated with beetles during attacks on trees. In this study, we found that beetles locate E. polonica and other fungal symbionts using volatile signals produced by fungal metabolism of tree resin.
CREDIT
Dineshkumar Kandasamy and Veit Grabe (CC BY 4.0, https://creativecommons.org/licenses/by/4.0/)
In your coverage, please use this URL to provide access to the freely available paper in PLOS Biology: http://journals.plos.org/plosbiology/article?id=10.1371/journal.pbio.3001887
Citation: Kandasamy D, Zaman R, Nakamura Y, Zhao T, Hartmann H, Andersson MN, et al. (2023) Conifer-killing bark beetles locate fungal symbionts by detecting volatile fungal metabolites of host tree resin monoterpenes. PLoS Biol 21(2): e3001887. https://doi.org/10.1371/journal.pbio.3001887
Author Countries: Sweden, Germany, South Africa
Funding: Financial support was provided by the Max Planck society to DK, RZ, YN, HH, AH and JG. MNA acknowledges funding from the Swedish Research Council FORMAS (grants #217-2014-689 and #2018-01444) the Crafoord foundation, the Royal Physiographic Society in Lund, and the Foundation in Memory of Oscar and Lily Lamm. The funders had no role in study design, data collection and analysis, decision to publish and writing.
JOURNAL
PLoS Biology
METHOD OF RESEARCH
Experimental study
SUBJECT OF RESEARCH
Animals
Fungi that causes pine ghost canker
detected in southern California trees
Pathogen native to US. but had not infected pines until recently
Peer-Reviewed PublicationIMAGE: THIS TREE IS INFECTED WITH THE FUNGAL PATHOGEN THAT CAUSES PINE GHOST CANKER, WHICH CAN BE FATAL FOR TREES. view more
CREDIT: AKIF ESKALEN, UC DAVIS
Fungal pathogens that cause die-back in grape, avocado, citrus, nut and other crops has found a new host and is infecting conifer trees causing Pine Ghost Canker in urban forest areas of Southern California.
The canker can be deadly to trees.
Scientists from University of California, Davis, first spotted evidence that the pathogens had moved to pines during a routine examination of trees in Orange County in 2018. Over four years, they found that more than 30 mature pines had been infected in an area of nearly 100 acres, according to a report in the journal Plant Disease.
Akif Eskalen, a professor of Cooperative Extension in the Department of Plant Pathology at UC Davis, suspects drought and other stress conditions brought on by climate change weakened the tree species, making it more susceptible to new threats.
“We have been seeing this on pine trees for the last several years,” he said. “Our common crop pathogens are finding new hosts.”
Pine Ghost Canker – caused by the fungal pathogens Neofusicoccum mediterraneum and Neofusicoccum parvum – usually infects the lower part of a tree’s canopy, killing branches before moving on to the trunks. This dieback in some cases can be deadly.
Points of entry
The pathogens infect a tree by entering through wounds caused by either insects, such as red-haired pine bark beetles, or pruning – meaning trees in managed or landscaped areas could be at risk. Another route is via tiny natural openings known as lenticels that fungi can make their way through, said Marcelo Bustamante, a Ph.D. candidate in Eskalen’s lab who is first author on the paper.
Spores from the fungi can disperse and the higher the prevalence means an increased chance of transmission. Rain, irrigation water and humidity by fog can trigger the right circumstances for the spores to spread, he said.
“The detection of these pathogens in urban forests raises concerns of potential spillover events to other forest and agricultural hosts in Southern California,” Bustamante and others wrote in the report.
Dead branches can indicate a canker. Detecting the fungi is not an emergency but “people should keep an eye on their plants when they see abnormalities,” Eskalen said.
Cankers are localized areas on stems, branches and tree trunks that are usually dead, discolored and sunken. On bark, the spores can look like strings of discolored dots.
The lab has posted a brochure about how to best manage wood canker diseases. Tips include:
- Keep your trees healthy: Proper irrigation and maintenance will keep trees strong.
- Prune dead branches to reduce sources of infestation.
- Avoid unnecessary pruning, perform structural pruning only.
Karina Elfar, Molly Arreguin, Carissa Chiang, Samuel Wells and Karen Alarcon from the Department of Plant Pathology contributed to the paper, as did experts from Disneyland Resort Horticulture Department, State University of New York’s College of Environmental Science and Forestry, UC Irvine and UC Los Angeles.
Spores of a fungal pathogen capable of causing Pine Ghost Canker is on the surface of bark.
CREDIT
UC Davis
JOURNAL
Plant Disease
ARTICLE TITLE
First Report of Neofusicoccum mediterraneum and Neofusicoccum parvum Causing Pine Ghost Canker on Pinus spp. in Southern California
