Mycorrhiza in coastal dune ecosystems: an overview

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MSc Earth Sciences

Geo-Ecological Dynamics

Mycorrhiza in coastal dune ecosystems: an overview

Casper Borgman

Student nr. 10556583

11 October 2019

12 ECTS

August-October 2019

Supervisor: A.M. Kooijman

Co-assessor: F.T. de Vries

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Summary

The symbiotic relationships between plant and fungi, mycorrhizas, are difficult to study and their overall contributions to ecosystems are largely unknown. Mycorrhizas can alleviate nutrient and climate stress, provide protection against plant pathogens. On the other hand, they can also be detrimental to either the plant or the fungus. This literature review

summarises the behaviour of mycorrhizal relationships in coastal dune ecosystems, with a slight focus on coastal dunes in the Netherlands. These dunes show a variety of properties, such as differing pH and phosphorus(P) and nitrogen(N) availability to plants. The role in dune stabilisation is examined, as well as the aforementioned pH, P and N availability, the physical protection and resilience to climate change.

An indication is found that mycorrhizal relationships aids in the stabilization of soil and promotes vegetational succession. Arbuscular mycorrhiza is mainly present in nutrient poor and lime rich situations and mainly provides alleviation of nutrient stress. Other kinds of mycorrhiza such as ericoid mycorrhiza and ectomycorrhiza become more common in more acidic soils where more nutrients are freed and more heavy metals are liberated. These provide protection against those heavy metals and to climate stress as well. However, fungi seem to be vulnerable to climate change, and the potential for the impact of climate change on fungi is underlined.

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Introduction

Mycorrhiza are an essential component of the natural environment of the whole planet. They determine in part the plant biodiversity, ecosystem variability and productivity (Van der Heijden et al., 1998). A mycorrhiza is classified as the symbiotic relationship between plants and fungi and can be found in the root system, also known as rhizosphere, of a plant. Mycorrhizal fungi are crucial in vegetation dynamics, as they facilitate nutrient uptake of nutrients such a phosphorous (P) and nitrogen (N). They function as an extension of the root system and sometimes are better at specific nutrient uptake than the host plant (Maun, 2009). Most of the terrestrial plant species form associations with mycorrhizal fungi (Smith & Read, 2010). Symbiosis can be either mutualistic, commensalistic or parasitic. In other terms, mutually beneficial, beneficial to one species with no negative effects for the other, and beneficial for one species with a negative impact on the other species. Most

mycorrhizae are involved in a mutualistic symbiotic relationship. Many laboratory studies have been conducted to examine the effects of mycorrhiza on host plans, however there is still a lot unclear about specificity and distribution of mycorrhizal fungi in the field or how they affect vegetation dynamics (Kowalchuk et al., 2002).

Coastal dunes are areas crucial to coastal defence and often are characterized by high vegetation dynamics. The sand of the dunes is often in motion and the way a dune moves through a landscape is often dependent on the dominant wind direction (Bird, 2011). Specifically, coastal dunes form when there is a deposition of sand by the ocean that

subsequentially blows land inward. These dunes become more stable the more they are land inward, and land inward dunes are characterised by late succession stages of

vegetation such as forests. A differentiation can be made between primary and secondary dune groups. The primary dune groups have sand added by the beach, whereas the secondary group has sand deposited originating from the primary dunes. The soil

characteristics of dunes change over time as well, in for example nutrient availability and lime content (Kooijman and Besse, 2002).

The effect of mycorrhiza in these areas is largely unclear. Dune areas differ in what kind of vegetation they have and stability all dependent on their situation, succession stage and the presence of certain elements such as calcium carbonate. Mycorrhiza influence the nutrients available to vegetation, and thus the vegetation that can settle in an area.

Therefore, it could have large impacts on succession. On the other hand, mycorrhiza might also be influenced by nutrient availability and the vegetation that is present.

Mycorrhizae can be subdivided into two subgroups: ectomycorrhizas and

endomycorrhizas (Moore et al., 2011). Endomycorrhizas penetrate the cell wall with their hyphae/mycelium whereas ectomycorrhizas do not penetrate the cells of plant roots. The fungi can be generalists, but some are only symbiotic with one genus of plants. In general, there are less species of fungi than plants. However, not all plants form a relationship with mycorrhizae. These plants are referred to as non-mycorrhizal plants (Moore et al., 2011).

As the way these subgroups interact with plants is different, there is also a difference in their occurrence in dune ecosystems. Generally, ectomycorrhizas are found near woody

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vegetation, as opposed to endomycorrhizas (Maun, 2009). Therefore, there should be different dynamics based on dune succession stage of an ecosystem as well as the soil composition that can be found in such an ecosystem.

Even though there is a proven interaction between mycorrhizal fungi and plants, one of the first studies regarding mycorrhizal relationships in a Dutch coastal dune ecosystem by Ernst et al. (1984) concludes that infection by one of the largest groups of fungi may be of little ecological importance to wild plants. They do indicate a large degree of uncertainty, which reinforces the need to summarise more recent literature to study the ecological importance of mycorrhizal relationships. The same study also points out how seasonal differences are clearly visible in mycorrhiza occurrence in the dune ecosystem. This raises the question how these differences might be impacted in the future by climate change.

This literature review focuses specifically on the impact of mycorrhizal relationships on dune vegetation dynamics, such as succession, seasonality, and nutrient availability. The research questions and aims are laid out below.

Research questions

As described in the introduction, important aspects of dune ecosystems are succession, dune movement, and seasonal differences. In addition, nutrient availability differs greatly depending for example soil pH. Mycorrhiza can alleviate nutrient stress, but as indicated by for example Ernst et al. (1984) the ecological significance is largely unclear. These

statements lead to the following research questions:

- What is the role of mycorrhiza in dune stabilisation and advancement of vegetation succession stages?

- What are the symbiotic/parasitic benefits and overall effects of the presence of mycorrhiza in dune ecosystems?

- What are the implications of a varying pH and varying nutrient availability on mycorrhiza?

o Specifically, regarding lime rich environments? o Specifically, regarding lime poor environments?

- What are the implications of climate change regarding mycorrhiza in coastal dune ecosystems?

The answers to these research questions will lead to a general overview of mycorrhizas in coastal dune ecosystems and will lead to fulfilment of the research aim.

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Methods

In order to provide consistent results this research uses a predetermined method of literature selection. All sources should be adequate and fulfil the criteria laid out below. In addition, this makes the research replicable and it tries makes sure no important sources are excluded of this research.

Study Area

Due to the nature of this literature review, there is no specific study area. However, the Dutch dunes are well studied in general and contain calcareous as well as more acidic dune systems, as well as the more dynamic foredunes and grey dunes. Therefore, many tie ins will be made using the dunes of the Netherlands as example.

Methods how sources of information have been selected

All sources have been found using search engines made specifically for indexing scientific literature. Specifically, Web of Knowledge, Google Scholar, and the University of Amsterdam library catalogue have been used in this research.

Selection criteria of papers

After using the scientific literature indexing and searching services, papers will be selected on the following criteria:

- The main topic involves mycorrhizal relationships between plant and fungi. - The study is in English. Some exceptions are made for studies in Dutch pertaining

information about the study area.

- Only scientific literature and official sources are used. Grey literature will be excluded. This included master’s theses.

- Papers about nonmycorrhizal fungi are excluded.

- Papers about dune ecosystems in general must be able to be related to coastal dune ecology.

There has been no exclusion based on impact factor of journals.

General method

The remaining papers are then read thoroughly, and relevant information pertaining to the research questions of this literature review will be summarised from each paper. After all the information is collected, the results are written down in the results section.

The methods laid out here are used for all sections except for the general information about fungi and mycorrhiza. Books and sources that summarise important and relevant

information have been used for this purpose.

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Results

Preliminaries

The division of mycorrhizas into two subgroups is quite simplistic for such a commonly occurring relationship between plants and fungi. Additional subgroups that are subdivisions of Endomycorrhizas and Ectomycorrhizas can be described: arbuscular mycorrhizas, ericoid mycorrhizal, orchidaceous mycorrhizas, arbutoid mycorrhizas, Monotropoid mycorrhizas, ectendomycorrhizas (Moore et al., 2011). An overview is given in table (1).

Table (1). Seven subdivisions of mycorrhizas. From: Moore et al. (2011).

Feature Mycorrhizal type

Endomycorrhizas Ectomycorrhizas Arbuscul

ar

Ericoid Arbutoid Monotropoid Orchid Ecto-

Ectendo-Fungi septate No Yes Yes Yes Yes Yes Yes Fungi aseptate Yes No No No No No No Intracellular

colonisation

Yes Yes Yes Yes Yes No Yes

Fungal sheath No Yes Yes or no Yes No Yes Yes or no

Hartig net No No Yes Yes No Yes Yes Vesicles Yes or

no

No No No No No No

Plant host chlorophyllus

Yes Yes Yes No No* Yes Yes

Fungal taxa Glomero -mycota Asco-mycota Basidio-mycota Basidio-mycota Basidio-mycota Basidio-mycota & Asco-mycota

Basidio- & Asco- & Glomero-mycota

Plant taxa** Bryo Pterido Gymno Angio

Ericales Bryo

Ericales Monotropa Orchida-ceae

Gymno Angio

* Orchidae are usually achlorophyllus in the early growth stages, chlorophyllus at adult stages. ** Bryophyta, Pteridophytes, Gymnospermae, Angiosperms.

As can be seen in this overview, there are some peculiarities to each subdivision. The septa of a fungus are the walls between cellular compartments that make up the hyphae. Thus, when a fungus is septate, these walls occur between individual cells. The septa allow the movement of fluids and molecules between them and sometimes count as supporting structures. Aseptate means that septa occur only at branching points of the fungus (Moore et al., 2019). The fungal sheath in mycorrhiza is what surrounds the plant root of the

symbiote. The Hartig net consists of hyphae growing inward into the root of a plant, through which nutrients can be exchanged (Becquer et al., 2019). Vesicles occur in the arbuscular mycorrhizas. They are swellings of hyphae that have a storage function that stores lipids and cytoplasm (Sullia, 1991). Chlorophyllus ability describes the ability of a host plant to create

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its own chlorophyll, thus whether they are dependent on mycorrhizas to create their nutrition (Cameron et al., 2009).

Furthermore, the overview shows which plant taxa the fungal taxa are often form mycorrhizal symbiosis with. The taxa that occur in for example the Dutch dunes are: Bryophyta, pterophytes, Angiosperms Gymnospermae, Monotropa, Orchidaceae (De Roos, 1980; Roobeek & Spruit, 2012; Maun, 2009).

The arbuscular subdivision is one of the most common mycorrhizas. It is used often in agriculture for increased nutrients uptake, specifically in P uptake. In dunes they are the most common and have many different types (Peterson et al, 2004). The arbuscular mycorrhiza forms a mycelial network around the root cortex that has vesicles as a main characteristic (bladder-like structures) along with arbuscules (branched finger-like hyphae) (Sullia, 1991).

Ericoid mycorrhizas are most often found alongside species belonging to the Ericaceae family of plant species and trees. These are often woody shrubs and heather related species. Characteristic for these mycorrhizas is that these mostly grow in very climatic and edaphic stress (Read, 1991). Thus, in soils that are very poor in nutrients and often have little water retention, such as sandy soils. In general, ericoid mycorrhiza are resistant to (pollution from) metals in the soil (Bradley et al., 1982).

Arbutoid are restricted to plant taxa of Ericales (Moore et al., 2011; Maun, 2009). In dune ecosystems they form mycorrhizas with Arbutus, Arctostaphylos and Pyrola. They are characterized by the production of a Hartig net and are therefore similar to

ectendomycorrhizas (Maun, 2009).

Monotropoid mycorrhiza are different from arbutoid mycorrhiza in the sense that they never penetrate plant cell walls, whereas arbutoid mycorrhiza do. Often times, the fungus transports carbon from one source, such as a tree, to a plant from the

monotropaceae family (Moore et al., 2011). These species of plants are rare and often protected. They do not produce their own chlorophyll. One example that occurs in dune ecosystems is the Monotropa Hypopitys, which occurs near angiosperms such as the Salix

repens (Roobeek & Spruijt, 2012).

Orchids in their seedling stage are always dependent on mycorrhiza to grow, as the seeds do not contain a lot of nutrient reserves and they are often achlorophyllous at this stage. Just like the monotropoid mycorrhiza, the orchid mycorrhiza transport carbon and nutrients to the orchid. However, the fungus can also drain too many nutrients from the orchid, so that it will never germinate (Moore et al., 2011). In general, orchids are not keystone species for an ecosystem and the mycorrhizal relationship between orchid and mycorrhiza is sometimes limiting due to specificity (Bidartondo et al., 2008) and sometimes not limiting (Waud et al., 2017). The presence of these mycorrhizas is often determined by ecosystem wellbeing and orchids are used as indicators of this wellbeing; however, the effects of their presence are limited. Therefore, in depth analysis is excluded.

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Ecto- and ectendo-mycorrhiza are both similar to each other. The only significant difference is that ectendomycorrhizas penetrate living cell plant cells as well as dead ones. They are often found near tree species associated with the gymnospermae and angiosperms (Moore et al., 2011). Within dune ecosystems this means that they are often found in the later stages of succession.

Plants that don’t form a mycorrhizal connection are called nonmycorrhizal plants. They are capable of surviving on their own and thus self-sufficient. However, they are indirectly influenced by mycorrhizal plants for a variety of reasons. They can be direct competitors to mycorrhizal species of plants as one example. In any case, they are part of the plant communities often existing out of nonmycorrhizal and mycorrhizal plants and thus can form complex relationships based on the plant community.

One such complex relationship is nutrient distribution across multiple plants through the fungal network. Carbon has been shown to move from paper birch trees into Douglas-fir trees thereby promoting succession in ecosystems (Simmard et al., 1997). Sometimes plants are linked and an exchange of C between plants happens, to the detriment of the donor but to the benefit of the receiver. However, there is much unclear about this still (Smith& Smith, 2003). Carbon and other nutrients allocated to the fungus or to the other plant is only a cost if it would have been used to increase the plant fitness, and the nutrients gained from the fungus are only beneficial if they are otherwise limited (Johnson et al., 1997).

For all the mycorrhizal species the following is true. The response of the host plant determines the success of the mutual relationship. The roots should be able to host the fungus, e.g. a connection needs to be made and then the ability of the plant to exchange nutrients and photosynthates with the fungus determines further success. Also important is the ability of the fungus to develop a mycelium into a large volume of soil (Maun, 2009). Furthermore, Moore et al. (2011) indicate that fungi can provide root pathogen protection due to physical barriers and interactions with microorganisms.

Mycorrhiza in coastal dune ecosystems

P and N are essential minerals required for plant growth. Mycorrhiza help with the uptake of these nutrients, as well as other nutrients such as Carbon (C) if for example the plant species is achlorophyllous or in extreme circumstances where not enough is available through the air via CO2. However, these two are the main limiting factors often inhibiting plant growth. A limited amount of either one will inhibit plant growth. Usually, low mobility of phosphate ions restricts P availability (Walker and Syers, 1976). The availability of the compounds of these elements depends on pH, but also on the amount that is already present in the soil and the exchange in and out of the soil. Main drivers for ecosystem functioning and nutrient cycling are soil organic matter (SOM) and pH. However, these both change with time due to soil development and succession, and thus change how P is available in the soil (Walker and Syers, 1976). Both processes are of great importance in dune development.

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The Dutch dune can be subdivided into two districts: the Wadden district and the Renodunaal district. Dunes normally have a varying pH gradient based on location, newer dunes often have a higher pH as high as 7, whereas older dunes more inland are more acidic, with a pH as low as 4. In addition, the districts the coastline is divided in are also characterised by a pH gradient due to differences in material deposition. The Wadden district has low lime, aluminium and iron contents, so that the pH gradient that naturally occurs is virtually non-existent; soils are tend to become more acidic at a faster rate. The Renodunaal district does show this pH gradient more clearly, and is rich in lime, aluminium and iron (Kooijman et al., 2009). There are other factors that also determine soil

composition in dune ecosystems. These factors include the stage of successions, the position (elevation and situation), nutrient loading and deposition from outside of the ecosystem, biotic factors (e.g. presence of cattle) and other abiotic factors.

In general, soils become more acidic / less alkaline the further away from the beach and with further succession stages in the chronological sequence. Kooijman et al. (2014) indicate that in calcareous Dutch dunes there is an indication of P-limitation in general. In more decalcified middle dunes, there seems to be more P available (Kooijman and Besse, 2002). Around a pH of 5, P is most solubility is highest, while the pH is not low enough for the aforementioned binding of P to iron and aluminium (Lindsay and Moreno, 1966). In older hinterdunes, which often have a lower pH, the availability of P is largely dependent on the presence of iron and aluminium, but on soil organic matter as well. Iron and aluminium presence decrease availability of P to plants, whereas increased SOM increases P availability (Lindsay and Moreno, 1996; Gu et al., 1994). Thus, if a soil becomes more acidic more P becomes available. In addition, N is deposited from the air into the soil and fixated by bacteria continuously. The result is a positive feedback loop, as vegetation is not limited by nutrients, more organic matter is deposited into the ground, organic matter binds itself to lime, freeing more P and causing the soil to become more acidic, thus further removing growth limitations by P and N. There are ways to combat this feedback loop, such as removal of vegetation and reintroducing blowout dynamics into the dunes. However, understanding the response of mycorrhiza to a pH gradient and P and N availability can attribute to a better understanding of the ecosystem.

Role of mycorrhiza in dune stabilisation and succession

Coastal foredunes specifically are characterised by the colonization of and then succession by replacement by other plant species. First the colonizer, usually with clonal growth form, colonizes the sand. After that, it reaches optimum growth, and then degeneration. As abiotic conditions change, other plant species can settle and outcompete the original vegetation. Especially clonal species are susceptible to pathogenic fungi, and thus to being outcompeted as well (Brussaard et al., 2001).

Arbuscular mycorrhizas are important for many pioneer species in the dunes. Many pioneer species in coastal dunes, especially stabilising species, are woody species such as the gymnosperms. Species belonging to the gymnosperm group are for example conifers such as pine trees, and fir trees. The arbuscular mycorrhizas allow the host plant to colonize

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new areas faster, due to faster seed output and faster biomass growth (Corkidi & Ricón, 1997). Some species even have lower survival percentages when they colonize without arbuscular mycorrhizas. Koske and Polson (1984) show a difference of 58% in survival rates from 78% to 20% surviving individuals of American Marram Grass Ammophila Brevigulata. One other benefit that helps colonizing plant species is the fact that the hyphae of

arbuscular mycorrhizas can adapt to shifting sand faster than a plants root system can. For example, when sand buries part of a plant, hyphae can grow upwards into this new

substrate (Perumal & Maun, 2006). Parallels with European marram grass can be drawn (De Rooij et al., 1995).

In addition to the fact that arbuscular hyphae can adapt to shifting sand, the presence of mycorrhizal fungi influence the formation of aggregates in the soil as well. Sutton and Shephard (1976) show that the soil adhering to a mycorrhizal plant is roughly three times greater compared non-mycorrhizal plants. In this case, the effect was caused by endomycorrhizal plants, of which arbuscular plants are a part of. The effect could be

different for other types of mycorrhiza. Miller and Jastrow (2000) indicate that the same effect is also caused by arbuscular mycorrhizal fungi in sand dunes. However, they also indicate that the effect becomes less important in more developed soils as well as more clayey soils, in which abiotic aggregation becomes more important. The effect of arbuscular mycorrhizas is especially noticeable between the micro and macro-aggregate level. The mycorrhiza helps the micro-aggregates bind to other micro-aggregates to form macro-aggregates. More stable aggregates provide more stable conditions for colonising vegetation species

Vascular plants and specificity of mycorrhiza pairing greatly depend on the pH and nutrient availability and SOM. Especially vegetation has a preference for a certain pH at which it grows best. The nutrient uptake strategies of plants depend on these factors, and can partly determine vegetation patterns (Lambers et al., 2008). The variety of fungal mycorrhiza species is closely related to the P uptake from the soil. When more species of fungal mycorrhiza are present, there is a lower amount of P below ground and more P in plant matter above ground (Van der Heijden et al., 1998; Koide, 2000). There are different kinds of mycorrhizal plants that exploit a variety of sources of P (Smith et al., 2011).

Nematodes and soil borne diseases can threaten colonization of colonizing species or influence the succession of the vegetation. Van der Putten et al. (1992) show that soil-borne diseases and for example nematodes are heavily involved in this process as well. These are also dependent on abiotic conditions, however they do appear to synergise with specific fungi. In Dutch marram grass, De La Peña et al. (2006) show that the introduction of

arbuscular mycorrhizal fungi significantly reduced nematode infestation. Fitter and Garbaye (1994) support that certain mycorrhiza interact and even synergise with soil bacteria,

sometimes to the detriment of the host plant. This is due to hyphal grazing on the fungus by soil animals on external mycelium. In addition, parasitic microorganisms and micro fauna can contribute to the destruction of hyphae (Smith and Read, 2010). However, the research of Fitter and Garbaye (1994) indicates mycorrhizas also protect root systems. Some fungi produce antibiotics whereas some produce antimycotics. Antibiotics degrade the cell

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membranes of bacteria, whereas antimycotics degrade the cell membranes of fungi. In addition, the coating of the fungus on the roots provides a physical barrier around the plant roots. Furthermore, the fungus can influence microorganisms that limit pathogens. In particular, ectomycorrhiza protects roots effectively. (Moore et al., 2011).

On the other hand, it seems that root structure of some sand dune vegetation in the Netherlands does not adapt significantly towards arbuscular mycorrhiza in most aspects due to entering a mycorrhizal relationship. In a few parameters, such as root length and

root/shoot ratio, significant differences were noticed when comparing 13 common sand dune species in a mycorrhizal and non-mycorrhizal state. These differences could

sometimes even be coincidental as well and don’t occur in all observed species. Instead, different plant root developments were observed between relationships with different mycorrhizal species. This could mean that changes in root systems are effects of mycorrhizal fungi instead of plant adaptation to fungi (Unger et al., 2017).

Mycorrhiza in lime rich coastal dunes

Arbuscular mycorrhiza mainly enhances uptake of P but also that of N. These are the most common in lime rich dunes, most likely due to the inorganic P in the soil that is still not very soluble (Maun, 2009). Smith et al. (2000) indicate that a difference in abilities of individual arbuscular fungi could have a strong impact on vegetation growth capabilities for P-limited soils. The availability of P to arbuscular mycorrhizal fungi in specific has been shown to be very important to hyphal growth and in particular spore production. This is indicated separately by Sivakumar (2013), Liu et al. (2016) and found in a sand dune case study by Moradi et al. (2017). In very P-limited situations, spore production is severely limited. This could relate back to initial soil conditions in coastal sand dunes and negatively influence colonization and succession of plant species.

In both nitrogen and phosphorus limited situations, such a primarily in lime rich coastal dunes, nitrogen fixing bacteria have been shown to benefit from P uptake from mycorrhiza to the plant, which in turn benefits mycorrhizal growth. Determining the exact workings of these intertwined systems would involve removing the mycorrhiza from the plant system without any harm done to other organisms. This is very difficult to achieve, and no technique is available for this yet (Fitter and Garbaye 1994).

Even though this is difficult to study, it is clear that changing soil conditions such as a change in pH sometimes lead to degeneration of one vegetation community, whereas it can provide opportunities for others. Kowalchuk (2002) performed research into the

relationship between marram grass A. arenaria, and arbuscular mycorrhiza that indicates that declined plant health due to changing soil conditions could negatively impact the infestation of arbuscular mycorrhiza, and thus increase susceptibility to plant pathogens. They observed different mycorrhiza sequences between different sites that had differing population health. In addition, total successful arbuscular mycorrhiza infection declined between healthy and degenerating marram grass stands.

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Furthermore, Johnson (1993) tests the hypothesis that fertilisation of soil,

comparable to what happens naturally when pH slowly decreases, impacts the relationship of arbuscular mycorrhiza with their host plant. Their research supports that when the soil is increasingly fertilised, fungi that are less beneficial mutualists are more often present. In addition, the carbon cost to the plant host increased, while the amount of nutrients supplied to it decreased. The selection of less beneficial fungi in this case can have implications for the nutrient availability when a certain nutrient becomes less available through for example decreased input (Johnson, 1993). However, plants may be able to adapt their dependence on arbuscular mycorrhiza based on soil conditions (Schulz, 2001).

Somewhat contrastingly, in a study on the effects of pH on a grass species, Oryzopsis

hymenoides, Al-Agely and Reeves (1995) found that there was a strong negative correlation

between arbuscular mycorrhiza formation and increases in pH and soil moisture. Indicating that an increase in pH would lead to a decrease in mycorrhiza formation. This was found using a regression analysis of bioassays.

The transition of so-called white dunes to grey dunes can be impacted by the extent of the arbuscular mycorrhizal community. The presence of an extensive arbuscular mycorrhizal networks can have antagonistic effects on seedlings of invading species that do not form beneficial relations with these arbuscular fungi. (Koske and Gemma, 1997). This is

dependent on the inoculum potential. Active exclusion of nonmycorrhizal and mycorrhizal plant species with high specificity can occur when the inoculum potential is high (Francis and Read, 1995).

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Mycorrhiza in lime poor dunes

In lime poor dunes and dune slacks some of the vegetation species are from the Ericaceae family, which are well adapted to more acidic growing conditions. It has been shown that the earlier mentioned ericoid mycorrhiza is especially adapted at relieving environmental stresses, such as providing nutrients in more acidic conditions and protection against heavy metals. There are a great variety of adaptations in these kinds of fungi, however this is one of their common denominators. This could explain part of the species variety found in this habitat (Cairney and Meharg, 2003). Nonmycorrhizal plants are more common in acidic and older dune ecosystems, also likely related to P availability. (Maun, 2009). There is a clear distinction between arbuscular and ericoid and ectomycorrhizal plants. Ericoid and ectomycorrhizal plants take up nutrients from organic sources, whereas arbuscular and nonmycorrhizal plants obtain more from inorganic sources of P (Read, 1989).

Dune valleys and slacks are often collection points of dead organic matter and are closer to the groundwater table than actual dunes. However, there is a great variety in these systems depending on soil and elevation, amongst other factors. Dune valleys are

predominantly inhabited by plants that are infected with ectomycorrhiza, such as salix

repens (Read, 1989). Furthermore, a variety of orchid species is dependent on the

calcareous and wet conditions often found in dune slacks. These species are dependent on the presence of a fungus they can form a mycorrhizal association with, however these can be generalist orchid mycorrhiza. For example, Liparis loeselii is not dependent on a specific species of fungus to germinate and grow. This could be because fungi do not tolerate very wet conditions very well (Waud et al., 2017). In any case, the aforementioned paper by Cairney and Meharg (2003) does help explain the survival of ericoid mycorrhiza and

Ericaceae related species in an environment as diverse as dune slacks are. Even though Read (1989) indicates that in dune slacks ectomycorrhiza and ericoid mycorrhiza occur primarily, little literature is available to confirm this. For example, Van der Heijden et al. (2000), to the contrary, speak of arbuscular mycorrhizas common with other species near salix repens.

Along a pH gradient in the Netherlands, Brussaard et al. (2001) found that there was no significant correlation in the functional composition between mycorrhizas, plant species, and nematodes. This study included a location with Salix repens on the Dutch island of Terschelling. However, in one study area they found a positive correlation between species richness of ectomycorrhizal fungi and nematodes. They underline the importance of the interplay between mycorrhiza, nematodes and plants and the unknowns of functional redundancy in mycorrhiza and nematodes.

Other research shows that near salix repens communities along a pH and moisture gradient in the Dutch dunes neither moisture nor pH had a significant impact on the species richness of ectomycorrhizal fungi communities (Van der Heijden et al., 2000). This research excludes other hosts for ectomycorrhizal fungi, as salix repens was the only species that could host these in the community. Their research points to the yearly opportunity of both ectomycorrhizal and arbuscular fungi to compete for niches to explain the species variety, especially because the dune systems can be highly dynamic. What should be noted,

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addition to ectomycorrhizal (Van der Heijden et al., 2000). A follow up study indicates that ectomycorrhizas seem to provide the largest benefits to salix repens. This study also indicates that pH does influence the species compositions of mycorrhizal fungi somewhat, one species (hebeloma leucosarx) expanded its niche with salix repens when pH was higher (Van der Heijden and Kuyper, 2001).

A recent study by Friede et al. (2017) shows that P-fertilisation, such as what occurs when soils become more acidic, has no significant influence on plant and mycorrhizal biomass. This study is unique in the sense that they managed to create a temporal series using soil cores. The plants were N-limited, and the effect might have been enhanced by P-fertilisation. This study thus suggests that N-limitation impairs plant control over the mycorrhizal relation, such as over the resource attribution to the mycelium.

In the case of spore abundance and abiotic factors such as pH, Gemma et al. (1989) found no significant relation between abundance of arbuscular mycorrhizal fungi spores and these factors in a dune ecosystem. Instead, host characteristics and interactions with other mycorrhizal fungi seemed more important in spore abundance and sporulation.

As was mentioned earlier, when soils become more acidic, more heavy metals become bioavailable. Ericoid mycorrhiza is in general very resistant to heavy metals in the soil. Plants with ericoid mycorrhiza often contain fewer heavy metals than their

counterparts that are not infected with ericoid mycorrhiza. This has presented itself as a significant difference, even in plants that are vulnerable to heavy metals in the soil (Bradley et al., 1982). Bradley et al. (1982) propose that this is due to adhesion of the metals to hyphae. In any case they studied the influence of aluminium, copper, iron, lead and zinc. A more recent study shows that in some instances, ericoid mycorrhiza become resistant to metals, allowing soils that contain these to be colonized (Cairney and Meharg, 2003). Dueck et al. (1985) show for arbuscular mycorrhiza the resistance to zinc toxicity is increased when a plant is infected. Dueck et al. studied grasses in a polluted Dutch dune system for this effect. Especially in dune slacks and older grey and hinterdunes, in more acidic soils, the success of ecto-mycorrhizas and ericoid mycorrhizas in excluding metal ions and liberating P and N from acidic organic complexes is key in the success of the ericaceous species in their early succession stage (Read, 1989). Therefore, it could be that forming appropriate

symbiotic relations could be required for successional change in more acidic situations (Read, 1989).

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Climate change

Coastal sand dunes house very intricate ecosystems, highly impacted by outside changes as well as continually changing themselves. Changing climate will impact them in several ways, including but not limited to, changes in salt spray, temperature, and weather conditions and extremes as well as differences in shoreline retention due to rising water levels. These all influence the mycorrhizas present in coastal dune ecosystems as well (Maun, 1994).

The hyphal network of fungi represents a large carbon sink in the soil (Miller and Jastrow, 2000). Whether this is true for dune ecosystems is unclear. However, both organic matter and pH are important for ecosystem functioning and nutrient cycling (Swift et al., 1979). These are both influenced by climate change and pollution (Team et al., 2014).

Taking the Dutch coastal area as example; climate change is suspected to prolong the growing season, but more importantly cause more weather and temperature extremes, but wetter summers as well. Arbuscular mycorrhizas have been shown to promote

succession and colonization, however it is very sensitive to disturbance. Weather induced disturbance such as drought and often freezing and thawing, as well as mechanical disturbance and loss of vegetation are all factors it is sensitive to (Maun, 2009). Furthermore, Fakhech et al. 2018 show that if the daily low temperature increases, mycorrhizal attributes decrease. This study was carried out over three years, examining temperature, humidity and precipitation.

Sigüenza et. al (1996) indicate that for arbuscular mycorrhizal fungi an interesting difference can be seen depending on wet or dry conditions. During wet conditions, the mycorrhiza tend to form more arbuscules, whereas vesicles are more abundant when the soil was dry. This shows adaptability in arbuscular fungi to climate conditions. In addition, and somewhat contrastingly, this study indicates the colonization of American marram grass and European marram grass by fungi is heavily influenced by predominant wind direction and speed. Depending on conditions, fungal mycorrhiza only appear in a later growth stage of the grass. More weather extremes are thus expected to heavily impact this.

The fungi of mycorrhiza have been shown to sporulate at different times, often times this coincides with the host growing cycle (Gemma et al., 1989). As growing seasons change, so may the sporulation of mycorrhizal fungi. It is unknown whether this coinciding will continue to be synchronous with host plants, however.

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Discussion

One recurrence in literature is that the occurrence of mycorrhiza of all kinds is dependent on plant variety more than other edaphic conditions (e.g. Gemma et al., (1989), Brussaard, et al., (2001), Schulz, (2001). The general consensus seems to be that specificity to certain types of mycorrhizal fungi is not as important as plant specific habitat preferences. This is further strengthened by the belief that many mycorrhizal fungi fulfil the same main roles as other fungal species of the same genera, or in other words, there is a certain redundancy (Brussaard et al, 2001). This is reinforced by the findings that less mutually beneficial mycorrhiza is formed when there are more nutrients available in the soil (Johnson, 1993).

However, when looking at successional stages, there are indications that good symbiotic associations are required for successional change (e.g. Read, 1989). Furthermore, specific examples were found for coastal dune systems that show that

- Colonization rates are improved due to arbuscular mycorrhizas (Corkidi & Ricón, (1997); Koske and Polson (1984); Perumal & Maun, (2006))

- Mycorrhizas improve physical soil conditions, especially in sandy soils, for example by creating aggregates (Sutton and Shephard (1976) Miller and Jastrow (2000). - Mycorrhizas provide protection from pathogens and other soils organisms (Van der

Putten et al., (1992), De La Peña et al., (2006)). Sometimes to the detriment of the host plant (Fitter and Garbaye, 1994).

- Nutrient uptake is facilitated by mycorrhizal relationships but differs across mycorrhizal fungi species (e.g. Moore et al. 2011; Maun, 2009; Read, 1989) It remains largely unknown in which way these benefits of mycorrhiza alleviate plant needs; however, these are also assumed to be plant species specific.

General effects of mycorrhizal relations

All of the subdivisions given in table 1. occur in coastal dune ecosystems, even if not widespread. Especially monotropoid and orchid mycorrhiza are very specialised and show great specificity, however their ecological impact seems to little compared to arbuscular, ericoid and ectomycorrhizal species. As mentioned above, general effects are facilitating of colonization by vegetation species, improving physical soil conditions and providing physical protection from pathogens and soil organisms. There seem to be very little parasitic and detrimental effects caused by mycorrhiza, and they only seem to occur in already weak / degenerating ecosystems. However, it could be less well researched due to limited occurrence of this effect, whereas it still could have a profound effect. For example, in speeding up degeneration as indicated by Kowalchuk et al. (2002).

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Influences on succession

Especially arbuscular mycorrhiza seems to have profound impact on the colonization and succession of species. Depending on the composition of the mycelial network underground and other factors, however, either succession is impaired or facilitated by mycorrhiza. The general indicator seems to be that the effect is often facilitative, following vegetation suitability, as the mycorrhizal fungi release their spores mostly during growing seasons. Ericoid and ectomycorrhiza provide protection in more acidic soils against high amounts of heavy metals and therefore might be necessary for succession to occur.

pH gradient and nutrient availability

Generally speaking, arbuscular mycorrhiza occur more often at higher pH and provide the most benefits to the plants they accompany in these soils, of which one is marram grass. They are better at inorganic P uptake, and that is most likely the explanation for their increased occurrence at higher pH.

On the other hand, ectomycorrhizal species and ericoid mycorrhizas become more common in more acidic soils. P is more readily available, and there is less inorganic P in general. These mycorrhizal species are more adapted to these conditions. Another benefit is that these mycorrhizal species provide protection against heavy metals in the soil, that are also more bioavailable at lower pH. Another common result found is that nonmycorrhizal species occur more often in more acidic conditions. This could be explained by a higher groundwater table, which impairs mycorrhizal functioning.

Most studies seem to indicate the same relation here: the mycorrhizal network is dependent on vegetation as well as soil conditions. The presence of a pH gradient as well as a soil moisture gradient do not seem to impact mycorrhiza greatly. In one instance, not in the Netherlands, a higher pH meant that mycorrhizal attributes became less common. Van der Heijden et al. (2001) indicate that species composition of mycorrhiza is influenced by pH, instead of the other way around. Furthermore, Schulz (2001) indicates that plants can alter their dependence on mycorrhiza based on soil conditions as well.

However, it is shown that where more mycorrhizal species are present, there is less P in the ground. This indicates that the presence of mycorrhiza does an effect on nutrient availability.

Climate change

Especially ectomycorrhizal and ericoid fungi seem to protect plants against pollution. This effect is most pronounced in more acidic conditions, where for example heavy metals are more available. They allow a large variety of plants to endure harsh conditions and pollution of the soil. In addition to this endurance, these fungi might be necessary for germination of these species to occur in the first place.

Climate change can heavily impact the relationships between plant and fungi, and therefore all the before mentioned benefits and costs to plant and fungi. Fungi are sensitive

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to changes in temperature and wind. In addition, it is unclear how different growth cycles and different sporulation moments impact mycorrhizal relations.

Knowledge gaps

Limited information due to inability to isolate specific fungus and plant species due to dependence of most often the fungus on a host species. This is confirmed by many papers used for the results of this study, but is also confirmed by other recent studies involving mycorrhiza (e.g. Willis et al., 2016). There is no easy solution to this problem, and it will continue to influence research into mycorrhiza for the foreseeable future.

Because the plant-fungi mycorrhizal relationships are so intricate, not everything was examined for this research, especially if there was limited information available for dune ecosystems. For example, one strategy of some plants is to increase carbon deliverance to their associated mycorrhiza in P-limited situations, so that underground biomass of the fungus increases. This in turn increases P availability to the plant (Teste et al., 2016). However, limited information regarding these plant strategies was available for this case study on coastal dune systems.

Furthermore, limited amount of information on middle and grey dunes was found. Most research has been done into the first succession stages / first chrono sequence of dune ecosystems. Information on Salix repens communities was available, but not common for other communities in these later stages of succession. However, not unimportant are the effects of ecosystem retrogression as well as succession due to varying nutrient availability and the part that mycorrhiza play in this.

In addition, the focus of most studies was on the mycorrhizal relationship between fungi and plants. However, this means that the interaction between mycorrhizal and nonmycorrhizal plants has fallen to the background. This interaction can be an important factor in dune ecosystem, where dynamics can change rapidly.

Outlook

There is a lot still unknown about mycorrhizal relations in dune ecosystems, as shown by the knowledge gaps found during this research. Some studies seem to be limited by the amount of data that could be gathered (e.g. Van der Heijden et al., 2000 indicate this). In addition, as mentioned before in this discussion, methods of sample collections are often not good enough to isolate effects of for example solely pH on an isolated fungus or plant species. Especially if both are dependent on each other. These are problems that cannot easily be solved but can be alleviated by more funding and resource allocation to these kinds of research. However, this can only happen if the importance of mycorrhizal relationships is stressed. Even though 80-90% of all vascular plants can form relationships with arbuscular fungi (Moore et al., 2011), the curiosity about these intricate species relationships seems to be often lacking. During this research, many of the same authors were encountered, and recent research into coastal sand dunes in combination with this subject was lacking, indicating that this is not a well-researched field.

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This research has potentially indicated that even in dune systems there is a need for further research, as indicator and colonising species, amongst others, seem to be very dependent on mycorrhizal connections. Even when for example marram grass

encroachment becomes a problem due to nutrient overloading, it is still important to understand the ecosystem functioning as a whole when implementing countermeasures.

Furthermore, there seems be a clear knowledge gap regarding dune slacks and valleys, which often house protected and red-list species, which form intricate mycorrhizas as well (e.g. with orchids in anoxic conditions). These are not easily studied without

disturbing the species, however the protection of these species could be facilitated by filling knowledge gaps. This requires collaboration between microbiological and ecological

disciplines (Read, 1989).

Coastal sand dunes house many different species of plants and very intricate

ecosystems. What has become clear is that there is still a lot of knowledge to be gained in this field regarding data collection, sampling, analysis that will provide more insights into the mycorrhizal relationships many plants form in these ecosystems.

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Conclusions

The mycorrhizal relationships formed between plants and fungi are often beneficial in the coastal dune ecosystems. Mycorrhizal growth facilitates colonization of new species, succession of vegetation. Arbuscular mycorrhizal fungi provide nutrients and physical protection in different forms: e.g. the formation of stable aggregates as well as a barrier around the root system. Ericoid and ectomycorrhizal fungi are imperative for the survival and protection of many dune vegetation species in harsher as well as acidic conditions in the soil.

The fungi seem to be dependent more on plant and soil conditions than the other way around. Mycorrhizal composition and abundance are dependent on nutrient availability and pH. The variety and competition with other mycorrhizal fungi increases as more P is available in the soil. As pH increases mycorrhizal attributes are indicated to decline. The mycorrhiza often releases the most spores during the growth cycle of plants, allowing them to quickly adapt to the settlement of new vegetation species and to vegetation succession, also facilitating this succession. In some cases, succession is impaired due to maintenance of soil conditions and the infection on germinating seeds.

Even though they can be quick to adapt, changing conditions such as increasing

temperatures and weather extremes have been shown to in some cases heavily impact the success of mycorrhizal relationships, especially due to vulnerability of the fungi. Even though some fungi are resistant to pollution, climate change does seem to be a threat to these relationships.

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Mycorrhiza in coastal dune ecosystems: an overview

MSc Earth Sciences

Geo-Ecological Dynamics