**5. Significance of secondary metabolite production with respect to on-going climate change**

A number of environmental predictions of future global climate conditions are predicted in the fourth assessment of the United Nations Intergovernmental Panel on Climate Change (2007). The outlook included an increase in average temperature; an increase in intensity and length of droughts; an increase in global water vapour, evaporation and precipitation rates which will cause increasing tropical precipitation and decreasing subtropic precipitation; an increase in sea levels from glacial melt; and anthropogenic carbon dioxide production will further increase atmospheric carbon dioxide levels (Meehl et al., 2007). Most of these changes will have implications on the future adaptability and secondary metabolite production of lichen species. These secondary metabolites protect against increasing environmental stresses such as light exposure, water potential changes, microbial and herbivore interactions, and other changes associated with changes in environmental conditions.

Increases in temperature may require the increase of secondary metabolites such as salazinic acid to mitigate the effects of higher temperatures on lichen biology. The relationship between temperature and production of salazinic acid is thought to be related to the effect of hydrophobic properties of the metabolite. The metabolite, being produced by medullary hyphae, would ensure a hydrophobic environment to optimize carbon dioxide transfer to the algal cells. A higher temperature increases the water potential of the thallus and more need for hydrophobic conditions to allow optimal carbon dioxide exchange between air spaces and algal cells. However, a higher thallus temperature may also promote the initiation of transferring one algal partner for another partner. Depending on the taxonomic extent of different algal partners this may invoke different carbohydrate starting units or trigger a different biosynthetic pathway for secondary metabolite production. The predicted increases in average annual temperature in northern geographic areas may also promote temperate species of lichens to move further north into previously uninhabitable environments. Simultaneously, this may cause a more northerly movement of lichens that are adapted to or can tolerate cooler environments. The effects on epiphytic lichens will also be significant based on the availability of host tree species and how well the host trees adapt to climate change. Cool temperature plant species that do not adapt well to warmer temperatures may become fewer in number in northern regions. Fewer plant species may reduce the availability of suitable habitat for lichens specialized to growing on the bark of specific tree species. Species of lichens that are generalists, colonizing a number of different tree species or other substrata, will be better adapted to environmental changes than specialist species, because previously lost tree hosts may be replaced by succeeding species of plant host.

Droughts will further affect the plant community. Plants that are not drought resistant may become fewer in number and replaced by drought resistant species. Extreme drought may cause further loss of plants and increase soil erosion. Such a situation would create the opportunity for terricolous lichen expansion but perhaps on a scale too slow to prevent significant losses. Under the scenario of increased degree and frequency of drought, it might be expected that there will be an increased production of mineral chelating compounds and hydrophilic compounds; or institution of physiological mechanisms to retain water within the thallus. These physiological changes might be expected because rain would become less reliable as a source of water and nutrients.

**5. Significance of secondary metabolite production with respect to on-going** 

A number of environmental predictions of future global climate conditions are predicted in the fourth assessment of the United Nations Intergovernmental Panel on Climate Change (2007). The outlook included an increase in average temperature; an increase in intensity and length of droughts; an increase in global water vapour, evaporation and precipitation rates which will cause increasing tropical precipitation and decreasing subtropic precipitation; an increase in sea levels from glacial melt; and anthropogenic carbon dioxide production will further increase atmospheric carbon dioxide levels (Meehl et al., 2007). Most of these changes will have implications on the future adaptability and secondary metabolite production of lichen species. These secondary metabolites protect against increasing environmental stresses such as light exposure, water potential changes, microbial and herbivore interactions, and other changes associated with changes in environmental

Increases in temperature may require the increase of secondary metabolites such as salazinic acid to mitigate the effects of higher temperatures on lichen biology. The relationship between temperature and production of salazinic acid is thought to be related to the effect of hydrophobic properties of the metabolite. The metabolite, being produced by medullary hyphae, would ensure a hydrophobic environment to optimize carbon dioxide transfer to the algal cells. A higher temperature increases the water potential of the thallus and more need for hydrophobic conditions to allow optimal carbon dioxide exchange between air spaces and algal cells. However, a higher thallus temperature may also promote the initiation of transferring one algal partner for another partner. Depending on the taxonomic extent of different algal partners this may invoke different carbohydrate starting units or trigger a different biosynthetic pathway for secondary metabolite production. The predicted increases in average annual temperature in northern geographic areas may also promote temperate species of lichens to move further north into previously uninhabitable environments. Simultaneously, this may cause a more northerly movement of lichens that are adapted to or can tolerate cooler environments. The effects on epiphytic lichens will also be significant based on the availability of host tree species and how well the host trees adapt to climate change. Cool temperature plant species that do not adapt well to warmer temperatures may become fewer in number in northern regions. Fewer plant species may reduce the availability of suitable habitat for lichens specialized to growing on the bark of specific tree species. Species of lichens that are generalists, colonizing a number of different tree species or other substrata, will be better adapted to environmental changes than specialist species, because previously lost tree hosts may be replaced by succeeding species

Droughts will further affect the plant community. Plants that are not drought resistant may become fewer in number and replaced by drought resistant species. Extreme drought may cause further loss of plants and increase soil erosion. Such a situation would create the opportunity for terricolous lichen expansion but perhaps on a scale too slow to prevent significant losses. Under the scenario of increased degree and frequency of drought, it might be expected that there will be an increased production of mineral chelating compounds and hydrophilic compounds; or institution of physiological mechanisms to retain water within the thallus. These physiological changes might be expected because rain would become less

**climate change** 

conditions.

of plant host.

reliable as a source of water and nutrients.

Increasing carbon dioxide and atmospheric nitrogen levels may negatively affect lichen species overall. Being poikilohydric organisms, their passive absorption of air, water and substrate nutrients will be impacted by increased acidity due to pollution. Past research has shown that ozone and carbon dioxide kill the photobiont, which ultimately kills the lichen. Some secondary metabolites have the ability to mitigate these effects and some lichens are better adapted to polluted environments than others. Increases in pollution will entail increases in secondary compound quantities that neutralize the negative effects of acidity with the lichen. Usnic acid is a compound found within lichens inhabiting acidic environments. Higher acidity from pollution will negatively affect these species because of usnic acid's limited ability to control acidity. However, basic substrates have the ability to buffer against acidification, which is the result of most types of pollution. This could mean that those lichens will be better able to adapt to increased acid levels than usnic acid containing lichens. On the other hand, lichens growing on basic substrata could be at risk from acidification of limestone causing deterioration of the substratum or a change in the pH to a pH that is intolerable by the lichen.

Pollution is also thought to be responsible for the increased levels of ultraviolet light caused by the loss of atmospheric ozone. Cortical compounds and other compounds within the thallus that offer protection to the sexual and asexual reproductive structures and photobionts, may ensure that those lichen species will have some protection from increase ultraviolet light. Species lacking those photoprotective compounds may endure degradation of photobionts and an increased frequency of mutations due to ultraviolet light exposure. Environmental stress may stimulate the production of cortical compounds in species that normally do not produce them; in species that do not produce them frequently; and in increased quantities for the species that already produce them.

If biochemical diversity decreases in response to climate change (Hauck, 2011), fewer secondary metabolites will be available for herbivore defense and, therefore, more grazing on lichen thalli will occur. Metabolites that would normally be lost to the soil, where they have an effect on growth of plants and microbes, may become reduced in type and concentration of metabolite. The lower concentration of the metabolites in the soil will have a reduced effect on growth of plants and microbes. This reduced impact will allow more microbes and plants to grow among mats of lichens and perhaps outcompete lichen growth sooner than would be expected. With fewer compounds there might also be less protection from ultraviolet light and a diminished ability for lichens to adapt to environmental changes that require secondary metabolites. However, fungi are plastic and may adapt in other ways or produce an array of different types of compounds with similar effects. This scenario of the production of other ecologically valuable metabolites may be plausible since so many gene paralogs have been reported (Table 1) that have no known associated function.
