Systemic fungal diseases in naturalplant populations

Anders Wennström Umeå 1993

Department of Ecological Botany University of Umeå

S-901 87 Umeå Sweden

AKADEMISK AVHANDLING

Som med vederbörligt tillstånd av rektorsämbetet vid Umeå Universitet för erhållande av filosofie doktorsexamen i ekologisk botanik kommer att offentligen försvaras fredagen den 5:e februari 1993, kl. IO.00 i hörsal C, Naturvetarhuset.

Examinator: Prof. Lars Ericson, Umeå

Opponent: Prof. Peter G. Ayres, Lancaster, England

OrganisationUMEÀ UNIVERSITETDISSERTATIONDepartment of Ecological BotanyS-901 87 Umeå, Sweden Date of issue

January 1993

Document name DOCTORAL

AuthorAnders Wennström

TitleSystemic fungal diseases in natural plant populations

AbstractThe purpose of this thesis was to study interactions between systemic fungal

diseases and perennial plants. Using the systemic rust Puccinia minussensis on the host plant Lactuca sibirica, and the rust Puccinia pulsatillae on the host plant Pulsatilla pratensis, this thesis focused on: (i) the effects of systemic diseases on their hosts (ii) host and pathogen responses to abiotic factors, (iii) the importance of life history strategies for understanding host-pathogen interactions, and (iv) the evolutionary consequences of living in close associations.

Results of greenhouse experiments showed that Lactuca sibirica had a high plasticity in growth, since it produced significantly more shoots in favourable than in unfavourable growth conditions. Both the disease levels and the number of healthy shoots (i.e. escape) were significantly higher under favourable conditions. Disease spread within the rhizome was found to be incomplete, and the risk of aecidial- infection decreased with distance from the parent. Furthermore, one isolate of the fungus had highest success and reduced the host plant biomass and shoot production more on the clone it was collected on compared to four other clones .

In the field, disease levels were found to fluctuate more at localities subjected to disturbance, the host and pathogen abundances were found to be in phase and the pathogen showed no delayed response to increasing host densities. The rust Puccinia pulsatillae on Pulsatilla pratensis showed no fluctuations between years, low infection rates, and disease levels were higher in ungrazed compared to grazed sites. There was no escape from the disease in this system.

A comparison of characteristics of different systemic fungi and hosts with different growth patterns indicated that the life history strategies of both host plants and pathogens need to be studied if the long-term consequences of host-pathogen interactions are to be predicted.

Key wordsSystemic diseases, rust, smut, Puccinia minussensis, Lactuca sibirica, Puccinia pulsatillae, Pulsatilla pratensis, lateral growth, abiotic factors, disease transmission,

Language ISBN Number of pages91-7174-744-3

English

Signature Date• r f t •

Systemic fungal diseases in naturalplant populations

LIST OF PAPERS

This thesis is based on the following papers, which will be referred to by their Roman numerals.

I Wennström, A. and Ericson, L. 1992. Environmentalheterogeneity and disease transmission within clones of Lactuca sibirica. Journal of Ecology 80:71-77.

II W ennström, A. and Ericson, L. The effect and transmissionof one isolate of the rust Puccinia minussensis on five clones of Lactuca sibirica. Manuscript

III Wennström, A. and Ericson, L. Population dynamics of therust Puccinia minussensis and its host plant Lactuca sibirica. Manuscript

IV Wennström, A. and Ericson, L. 1991. Variation in diseaseincidence in grazed and ungrazed sites for the system Pulsatilla pratensis - Puccinia pulsatillae. Oikos 60:35-39

V Wennström, A. Systemic diseases on hosts with differentgrowth patterns. Manuscript

Paper I and IV are reproduced with due permission from the publishers.

BACKGROUND

Parasitic fungi have been known by man since ancient times. There are references going back to some 4000 years BP, but pathogens were probably a problem soon after the domestication of crops. At first, plant diseases did not have names, and their origins were not understood. For example, in the 17th century Italy, a festival was given for the rust god, Robigus, where one dog painted red and one sheep were sacrificed. It was not until the 19th century that the associations between fungi and diseases in plants were established (Ainsworth 1976).

Pathogens have caused devastating effects to crops throughout history, e.g. the great famine in Ireland 1845-1846 was caused by heavy outbreaks of Phytophtora infestans, which destroyed the potato crops. This resulted in the death of half a million people, and 1.5 million people emigrated to America (Agrios 1978). Therefore, it is not difficult to understand that the emphasis in research on parasitic fungi has been on agricultural crops. Studies of interactions in natural plant populations have been few, except for a period at the end of last and the beginning of this century, when important work was done on the biology and taxonomi of pathogens in natural plant populations (e.g. Rostrup 1902, Clinton 1904, Liro 1924), and in which the secret of heteroecism was revealed (diseases that alternate between two or several plant species) (deBary 1865).

It was not until Harper (1977) and Price (1980) devoted chapters in their textbooks to pathogens, that ecologists generally became aware of pathogens and their role in natural plant communities. Up to that point, fungal pathogens had been regarded as being unimportant in natural plant communities and the prevailing belief was that epidemics were rare in nature since pathogens had coevolved with their hosts (van der Plank 1960). Now, pathogens have become fashionable and their effects are included in discussions about possible factors which are important for shaping plant populations and communities. Theoretical work has also appeared, which treat diseases as a group although their emphasis was on parasites on animals (Anderson and May 1979, Hamilton 1980, Levin and Pimentel 1981).

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Burdon (1987) was the first to tie the work from the applied fields of agriculture and forestry together with recent work done in natural plant populations. His book accentuated the fact that the work done on pathogens had been biased, in that concentration had been on short lived plants, and mainly crops which are attacked by non-systemic diseases. This bias is not totally relevant when working in natural plant populations, since other types of life-history strategies are common among plants and fungal pathogens. Another common bias is that the way to increase our knowledge about plant-pathogen interactions is through studies on virulence and resistance. The emphasis has been on frequency and number of resistance genes and their long-term fate in plant populations. Other questions such as: what are resistance for, what are the roles of abiotic factors in plant- pathogen interactions, and how important are life-history strategies of both host and pathogen, have not been addressed clearly. Recent literature indicates that attention is now being paid to these questions (e.g. Burdon and Leather 1990).

I have chosen to focus on an important biological group of pathogens, namely those that are systemic and cause perennial infections. These types of diseases have been largely neglected since the early part of this century, when much work was done (e.g. Woronin 1882, Plowright 1889, Liro 1908, Tischler 1911). During recent years, however, one specific group of systemic diseases have attracted much attention, namely the sterilizing anther smut (Microbotryum violaceum) (e.g. Jennersten 1988, Alexander 1990, Carlsson and Elmqvist 1992). However, the main group of systemic diseases are not anther sterilizing. They often deform stems and leaves and cause abortion of flowers. This large group has rarely been studied. In this thesis, I have concentrated on perennial systemic rusts and smuts on plants with strong lateral growth and focused on: (i) systemic diseases and the effects on hosts (ii) host and pathogen responses to abiotic factors, (iii) how life-history strategies of both host and pathogen change the patterns of interactions and (iv) the evolutionary consequences of living in close associations.

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OUTLINE OF THE PAPERS

Paper I. Plants with a strong lateral growth, and with ramets that are physiologically integrated throughout at least one season, may experience large differences in soil conditions over the length of the rhizome. In a greenhouse experiment, I studied the effect of uniform and patchy soil conditions on the growth on the the host L. sibirica, and also the response and distribution of its systemic rust, P. minussensis.

Paper II. Plant pathogens are often highly specialized by having one or a few species of plants as hosts. Adaptation to their hosts can also be seen on a more local scale, at the population level. Data show plants to be more susceptible to pathogens if they have grown outside the distribution range of the pathogen compared to plants grown within the local area of the pathogen (Hunt and Van Sickle 1984). In this experiment, I have studied the success and effect of one isolate of the pathogen P. minussensis on different clones of the host L. sibirica in comparison to the clone from which it originated.

Paper III. Both plants and pathogens respond to changes in the environment by, for example, enhanced or reduced growth. Therefore, environmental factors may be important in plant-pathogen interactions. In a field study, at localities subjected to accumulation or erosion, the effects of varying densities of L. sibirica for the disease P. minussensis were monitored during four years.

Paper IV. The system Pulsatilla pratensis-Puccinia pulsatillae was studied during three years. P. pratensis has in contrast to L. sibirica a weak lateral growth and is attacked by a microcyclic rust Puccinia pulsatillae. In this study, the disease levels, infection rates and survival of the host in grazed and ungrazed areas were monitored.

Paper V. To be able to develop a predictive theory of how fungal pathogens behave in plant populations we cannot just look at their effects on hosts without considering the different life history strategies of plants and pathogens. In this study, I have used six host-pathogen systems to evaluate the importance of host growth pattern for host response and disease expression.

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PATHOGENS - WHAT ARE THEY?

A pathogen or a parasite is an organism that lives on another organism (obtain nutrients etc.) and consequently causes some kind of negative effect on its host (Price 1980). Parasitic fungi enter plants in various ways, for example through the epidermis, roots or reproductive parts. Inside the plant, they live between the cells. Nutrients and water are transported out from a cell by haustoria that invaginate the cell membrane.

It is estimated that over 8000 species of pathogenic fungi exist (Agrios 1978). Pathogenic fungi do not form a homogenous group, and many different species belonging to different families are known to be pathogenic. Many different life strategies are found, among them:

systemic - a pathogen that lives within its host and is able to grow away from the site of infection to other parts such as leaves, and stems, and into roots, rhizomes and stolons. Some produce pustules along the way and some, e.g. Microbotryum violaceum on Silene dioica sporulates only in the flowers. Some systemic fungi are annuals, such as Puccinia violae on Viola spp. However, most of the systemic diseases produce a perennial mycelium after inoculation and survive within the plant during winter (Wilson and Henderson 1966). Many species of smuts are systemic, e.g. all species within the genus Ustilago in Sweden (Lindeberg 1959), many rusts, and most of the fungi belonging to the endophytes (Clay 1988).

non-systemic - a pathogen that lives in or on a host, but form localised lesions, i.e. it is not able to grow away from the site of infection. Non-systemic diseases are predominately annuals surviving as spores, and have to re-infect its host in the spring. Some rusts are believed to survive as mycelia within the plant (Wilson and Henderson 1966). Mildews and various rusts and smuts belong to this group.

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LIFE-CYCLES

The rust fungi are obligate parasites on plants. The rusts can be alternating (heteroecious), i.e. need two host species to complete their life-cycle, or they can be specific (autoecious), i.e. need only one host to complete their life-cycle. Most rusts produce five different spore stages (termed macrocyclic), but some rusts have deleted one or several spore stages. Those that only have telia (and spermogonia) left are called microcyclic (Petersen 1974) Fig. 1).

The smuts are obligate pathogens on plants. Most species form two spore stages, teliospores and basidiospores. The teliospores cannot infect hosts, but when germinating they form basidia from which basidiospores are formed. To be able to infect a host, two germinating basidiospore mycelia have to unite. Some smuts also produce conidia.

telia a basidia b

basidiauredia

spermogoniaconidia

aecia

Fig. 1. Life-cycle of (a) macrocyclic rusts and (b) smuts.

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STUDIED SPECIES

Host-pathogen system 1:

The pathogen.Puccinia minussensis Thiim., (Uredinales), is a macrocyclic rust specific to Lactuca sibirica in Sweden (Hylander, Jorstad and Nannfeldt 1953). We have found this rust in 19 of the 20 visited river valleys. It is systemic and able to spread within the rhizome of the plant. The aecia are produced on shoots emerging in early summer, and the yellow spores more or less cover the entire plant surface. Diseased shoots are thin and elongated, distortion of both leaves and stem is common and flowering is inhibited. Aeciospores infect new shoots which in July, develop uredospores. They are seen as scattered brown pustules on leaves and stems. From mid-August and onwards, the dark brown teleutospores are produced instead, but both uredo- and teleutospores can be seen on the same plant. The rust is systemic and survives within the rhizomes during winter.

The host.Lactuca sibirica (L.) Benth., (Asteraceae), is an alluvial species. It is distributed throughout Siberia and northern Russia and has its western limit in the Nordic countries (Hultén & Fries 1986). In Sweden, L. sibirica is a rare species, and only found in about 20 rivers from Selångersån in the south to Torneälv in the north. It inhabits mainly river valleys (dominated by Salix spp., A lm s incana and Prunus padus ) that are subjected to erosion and accumulation during spring flooding. L. sibirica is a clonal plant with a strong lateral growth (3.6m, own obs.) by means of slender rhizomes, which on suitable substrate can form extensive stands (Cajander 1909). It is an obligate outbreeder, hence viable seeds are not produced within populations. Pollination experiments have shown that seeds are not produced within river valleys, while seeds are readily formed when crosses are made between rivers (Wennström unpublished).

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Host-pathogen system 2:

The pathogen.Puccinia pulsatillae Kalchbr. (Uredinales) is a microcyclic rust fungus, in Sweden known to infect only Pulsatilla pratensis (Hylander et al. 1953). Gäumann (1959) lists several other Pulsatilla spp. as hosts from continental Europe and claims that the rust has a circumpolar distribution. P. pulsatillae is a perennial systemic fungus, surviving harsh environmental conditions in the host rhizome. Disease symptoms are seen during the spring and summer as brown lesions (telia) on the under surface of leaves. Infected leaves are born erect, while uninfected leaves remain postrate. According to Gäumann (1959) infected leaves wither later in the season than uninfected. The pathogen also inhibits flowering (Rostrup 1885). The mode of inhibition is not known to us.

The host.Pulsatilla pratensis (L.) Miller (Ranunculaceae) is a perennial dicotyledonous herb. The leaves are deciduous and the plant overwinters as a rhizome. The rhizome grows vertically, but branches so each individual may have up to 3-4 interconnected ramets growing closely together. Each rosette normally produces 1-2 floral shoots. Seeds are dispersed by wind with germination taking place during humid periods in autumn and spring.

In Sweden, P. pratensis is confined to the south east, where it is characteristic of dry calcareous grasslands (Andersson 1950). It is an European endemic, distributed over central and eastern Europe (Jalas and Suominen 1989)

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IMPORTANCE OF ABIOTIC FACTORS IN PLANT-PATHOGEN INTERACTIONS

Plinius (23-73 A.D.), was the first to point out the importance of abiotic factors in plant-pathogen interactions. He wrote about a rust "which cometh of some distemper of the air" and continues " this unhappy blast falleth most often in places subject to mists and dews, such as hollow valleys and low grounds" (cited after McAlpine 1910).

A number of studies have since identified various abiotic factors which are important in plant-pathogen interactions, such as light (Matson and Waring 1984), nutrients (Jenkyn 1977) and water (Ayres and Paul 1986). Changes in abiotic factors such as weather conditions can also have a profound effect on diseases. For example, humidity is very important for the germination of rust spores (Nighswander and Patton 1965, Kurkkela 1973), and thus has a strong direct effect on the pathogen. Non-systemic diseases are especially vulnerable since they have to establish new populations each spring. For these fungi, changes in humidity may speed up or slow down an epidemic. The effect of an abiotic factor can also be indirect by affecting the host. Application of nutrients results in an increase in disease incidence (Jenkyn 1977), suggesting that disease incidence is often linked to the nitrogen status of the plant (Paul 1990). Paul and Ayres (1986) also observed that the effects of Puccinia lagenophorae on Senecio vulgaris differed with nutrient supplies. Under stress plants were less affected by the fungus than under application of nutrients.

In my studies, I have shown that growing conditions affected the growth pattern of Lactuca sibirica (I, II). High nutrient potting compost enhanced the growth and spread of the rhizome, while unfertilised peat inhibited growth. When grown in a patchy environment, the plants showed a strong plasticity in growth by producing more shoots in high nutrient than in low nutrient patches. In comparison with uniformly high or low nutrient conditions, however, the shoot production was reduced and enhanced, respectively. The pathogen, Puccinia minussensis, was also found to respond to changes in nutrient availability. Plants grown in high nutrient conditions showed higher frequency of disease and higher numbers of diseased shoots compared to plants grown in uniformly

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low nutrient conditions. This was also true in a patchy environment. Although highest number of diseased shoots were found in high nutrient conditions, the highest number of shoots escaping the disease were also found here (I). I also observed a similar pattern in the field(III). Disease levels varied strongly between sites and between years, depending on growing conditions. In sites which were subjected to accumulation or erosion, the number of shoots decreased and so did the disease levels. In years when the plants were able to invade open areas, shoot density and disease incidence increased simultaneously.

EVOLUTIONARY CONSEQUENCES

Fungal pathogens are known to affect plant morphology and performance. Diseased plants may be elongated, distorted, stunted and sterile. For Puccinia minussensis I found that the spore stages had different effects on morphology of the host Lactuca sibirica. Aecia caused shoots to elongate and grow thin. Furthermore, these shoots did not flower and leaves and stems were often distorted. Uredia and telia, however, did not affect the morphology in this way (I, II). For Pulsatilla pratensis, the rust Puccinia pulsatillae, which is only producing telia, caused leaves grow erect, and flowering is inhibited(IV).

Host specific parasitic fungi and their host plants live in close associations (Harlan 1976). It has been argued that such systems ought to have coevolved so that adaptations of the host have triggered counter adaptations by the fungus. This should then result in reduced effects of diseases on the host and lower levels of disease (van der Planck 1960). In support of this hypothesis, studies have shown that plants within the distribution area of a parasitic fungus are more resistant than those outside the area (Hunt and Van Sickle 1984), and that populations subjected to high incidences of disease were more resistant than populations subjected to low incidences of disease (Snaydon and Davies 1972). Other studied, however, have indicated that fungal pathogens strongly affect their hosts, and high disease levels are commonly encountered in natural plant communities (e.g. Carlsson et al. 1990, Burdon et al. 1992). Furthermore, it has also been observed that a fungus can be adapted to one population of the host on a very local scale (Parker 1985). In my studies, high disease

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levels were found in infected Lactuca sibirica and Pulsatilla pratensis populations (III, IV), and one rust isolate was found to produce more diseased shoots on the clone it originated from than on four other clones (II). These data also suggest, that selection pressures on the pathogen do not necessarily result in more benign races.

The general features of systemic fungal diseases were dealt with in detail in paper V. Since these fungi are perennial and live within the plant tissue, they do not benefit from killing the host immediately. If the host is kept alive, sporulation can proceed over a number of years. Too strong an effect on the plant will not only lead to the death of the host it will also lower potential spore production and cause the ultimate death of the pathogen. However, as shown in paper V the effects of systemic diseases vary, not with the taxonomic position of the fungus, but with the life-history strategy of the host. A comparison of plants with weak lateral growth with plants with strong lateral growth suggests that the effect on shoots were, on average, less severe in plants with weak lateral growth than in plants with strong lateral growth. Reducing the vigour of a shoot can have a negative effect on the survival of the genet and consequently also of the fungus. This may be one reason why systemic diseases seem to enhance the growth of infected host plants (Clay 1988, paper IV). The effects on plants with strong lateral growth are often strong. Shoots are heavily diseased and in the case of Lactuca sibirica, aecia producing shoots die early in the season. For Trientalis europaea, conidia-producing shoots also die early in the season (Wennström and Ericson 1990). The strong effects found on ramets, however, do not necessarily have a negative effect on the survival of the genet, since there is only a weak correlation between ramet and genet survival (V).

Disease transmissionSystemic diseases, in contrast to non-systemic diseases, have the ability to spread within the plant tissue to other parts of the host. In many such systems, reproduction resulting in the production of seeds is the only means by which a plant may escape a disease, since systemic diseases are only rarely transmitted through seeds (but see Clay 1988). However, available data for diseases on plants with a strong lateral growth by stolons or rhizomes reveal that another means of escape exists, i.e. escape in space (V). For these diseases, the transmission within the host is incomplete. For example, only 33% of

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the buds produced by diseased mother plants of Trientalis europaea were diseased (Wennström and Ericson 1990) and similar escape has also been reported for Cirsium arvense (Bryzgalova 1928). For Lactuca sibirica (I), the number of diseased ramets decreased with the distance from the diseased parent plant, i.e. shoots produced further away from the parent plant had a higher chance of escaping the disease, and plants produced 45cm and further away were all found to be healthy. The mechanism behind this escape in space is not known, but in the case of L. sibirica, our data suggests that it is due to the growth of the rhizome (I). Whether other factors affect this escape is largely unknown, but recently, Johansson (1992) found that the size of ramets of Ranunculus lingua was an important escape mechanism from the downy mildew Peronospora gigantea. Escape mechanisms in space and time have rarely been studied, but may prove to be an important factor for plant survival, and for the balance between plants and pathogens. From the pathogens point of view, incomplete transmission may be selected for, since races of the pathogen capable of spreading to all of the ramets produced by a plant, will increase the risk of killing the entire genet, and consequently itself. Races of the pathogen that have a poor capacity to spread, will also run an increased risk of extinction, since the plant may outgrow the pathogen. Outgrowing the pathogen may also be an example of disease avoidance by a plant, i.e. it has been selected for in the plant population. Genotypes with long rhizomes and many shoots are likely to produce more shoots that will escape the disease and should be selected for. In the case of Lactuca sibirica,however, the genetic basis for selection does not exist within populations, at least in Sweden. The evidence for this is indirect, but powerful. I have never observed seed production within any of the 20 river valleys I have visited. Pollination experiments in the greenhouse also show that seeds are only produced when crosses are made between river valleys and not within (Wennström unpublished). This strongly suggests that the plants growing within a single river valley are members of a single clone, and hence, selection cannot occur. Production of long rhizomes may not always be the only way to escape a disease in space. For plants that produce short-lived connections that are formed close to the parent plant, I suggest that selection will favour more rapid formation and disconnection of the daughter ramets, for a successful escape from the disease (I), or a pathogen with a low virulence.

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Disease incidenceFluctuation in disease incidence is observed in many interactions between plants and pathogens (III). Three important factors causing fluctuations are: (1) life history of the pathogen, (2) life history of the host plant, and (3) abiotic and biotic factors.

The particular life history strategy of a pathogen may increase fluctuations in levels of disease. Non-systemic diseases are most often annuals, which means that populations pass through bottlenecks every year and spores have to reinfect the host population. This in itself creates fluctuations in disease levels within and between years (III). The life history strategy of systemic diseases, on the other hand, may stabilise disease levels. Since they live within the host plant from year to year, they do not pass through bottlenecks each year. However, abiotic factors tend to increase the instability of all systems, since changes in conditions often strongly affect the germination, establishment and growth rates of the pathogen. Thus, fluctuations in levels of disease may be observed even with the close association that typifies systemic diseases and their host plants. For example, it has been observed that disease symptoms are not expressed every year on plants with weak lateral growth. Pulsatilla pratensis attacked by the rust Puccinia pulsatillae, is free of symptoms some years, although the plant never flowers once infected (IV). Actaea spicata infected by the smut Urocystis carcinodes may abort diseased shoots at a very early stage and symptoms are not seen every year on infected plants (Wennström and Ericson unpublished).

For plants, there is a trade-off between sexual reproduction and growth. Sexual reproduction is costly for the plant and results in reduced growth (see e.g. Eis, Garman and Ebel 1965). Similar trade­offs are also likely to occur in the fungi (Pady 1939). Sporulation of the fungus may drain the host of resources. It has also been observed that disease levels increase with the application of nutrients, primarily nitrogen, and that the effect of disease on the host can be stronger after application of nutrients (Paul and Ayres 1986) Therefore, it has been argued that latency could be a response to low levels of resources and a way for the pathogen to avoid depleting the resources of the host, causing its ultimate death (II).

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For interactions where the plant responds strongly to changes in growing conditions, the latency of a pathogen could cause large fluctuations in disease levels. Lactuca sibirica has a strong lateral growth and responds quickly to changing environmental conditions. Under favourable growing conditions, the biomass and shoot production of this plant increases rapidly, while unfavourable conditions reduce biomass and shoot production considerably (I, II, III). The rust Puccinia minussensis responds to these changes in growth of the host, by having high sporulation when the growth of the plant is enhanced and low sporulation during years when the growth of the plant is hampered. This could be a response of the fungus to changes of resources in the host plant and/or an adaptation of the fungus not to kill the host. By living within the plant tissue, systemic diseases should be able to more directly respond to changes in die host plant population, with the result that die peak abundances of the host and the systemic disease are in phase. Non-systemic diseases, in contrast, are not perennials and subsequently they must regularly recolonize their hosts. This implies that the amount of inoculum available for building up disease epidemics reflects the disease incidence the previous year. Consequently the peak abundances of the populations of hosts and non-systemic pathogens are not in phase (HI).

CONCLUSION AND FUTURE STUDIES

In this thesis, I have shown that parasitic fungi are a diverse group of organisms. Even if we only consider systemic fungi, we find that they are not homogeneous in their behaviour in plant populations. Their effects on plant performance vary between systems. Therefore, if we are to understand the effects of parasitic fungi we cannot treat them as one large group. What I propose is that we should study the life history strategies of both pathogens and their hosts. By doing so, we will increase our understanding of host-pathogen interactions. What we need now is more data on different pathogens, with different life history strategies on plants with different growth forms and life history strategies. We also need more detailed information about the genetic variation in hosts and pathogens. Only in this way can general

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patterns emerge, and theories about how plant - pathogen interactions work be built up.

For the future, I find that several aspects of plant-pathogen interactions which have not yet been addressed, need to be studied in greater detail. For example, I believe that the work of geneticists and ecologists have to be brought together so that the right questions about ecological and genetica! aspects will be asked. Otherwise, the relevance of resistance and virulence in relation to other factors in plant populations will not be clear. Furthermore, as Harper (1990) pointed out, we still do not know what the pathogens are doing. Studies are performed where the pathogens occur and not where they are absent. Removal of pathogens, introductions of pathogens to new areas, introduction of plants to potential habitats are some important studies that still need to be carried out.

Interaction between plants-pathogens-herbivores is another field that workers with pathogens have not fully paid attention to. This, though data show that interaction between plants and pathogens really can be altered by adding a herbivore to the system. Herbivores may selectively avoid diseased or healthy plants (Potter 1987, Ramsell and Paul 1990), they may passively or actively spread diseases (Baker 1947, Ericson, Burdon and Wennström ms.) and they may affect interspecific competition (IV). Consequently the may alter the dynamics of both the host and the fungus populations. Interactions between several species of hosts that share a common pathogen, so called apparent competition (Holt 1977), also need to be considered in this context.

To conclude: Pathogens may prove not only to have a direct effect on plant reproduction, survival and distribution, but may also prove to be relatively important in an evolutionary context for selecting certain growth forms.

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Acknowledgement

To be able to write a thesis you need help. All types of help, both large and small contributions are appreciated and vital if things should work out well. First of all you need help from your study systems. If the plant or the pathogen is not co-operative things will not turn out well. (1) Plants can refuse to grow or grow when you want them to rest (Plasticity ?). Pathogens that you try to inoculate with, will not infect the host, while a pathogen that you are not interested in, is all over the place and eventually kills the host (competition ?). (2) Weather conditions (abiotic factors) can be difficult. It can be too cold (for me!) or a storm can demolish a nice set-up (as always) in hours; which is what happened after a couple of days planting of Rumex on Öland. (3) Knowledge. Capsella bursa-pastoris dies after flowering!

Secondly, you need people to help you and work with. First of all I would like to thank my supervisor Lars Ericson, or “lille" ( - “little") Lars as we call him at home, without whom this thesis would not have been possible. When I started at the department some people looked at me with pity. Lars has too much to do to be able to supervise students, they said. You will not see much of him. But Lars didn't know what he got into when he took me on as his student. I don't trust - "I come up to you later" as a promise, instead it is a backway out. The only way to get hold on him is by harassment. This lack of time by Lars is however outweighed 100 times by his enormous enthusiasm, knowledge of various systems, ability to find new problems, working capacity etc. This list that can be made very long, but to make it complete I have to add his appetite for ice-cream.

Another person that I need to thank is Jeremy Burdon. The author of the book I copied! (which didn't contain anything substantial about systemic diseases...) He has been a source of inspiration and help during this period.

There are several people at the department that deserves my thanks and all best wishes for the future. Some that I immediately think of are Ulla my room mate with whom I could discuss simple problems about the computer, and statistics that neither of us would ask anyone else, and all the gossip about the others. Hans, for being the source of all the gossip and help with keeping track of Lars. Tom, for being

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available for a fight and having distance to what he is doing. Åsa, for always being available for a chat. And all the rest of you that don't like to bang your heads in the wall.

Finally, I would also like to give many greatest thanks to Katarina for among many things being thg fungi and plant tracker, &£ greenhouse keeper, and MINE.

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References

Agrios, G.N. 1978. Plant pathology. Academic Press, New York.

Ainsworth, G. C. 1978. Introduction to the history of mycology. Cambridge University Press, Cambridge.

Alexander, H.M. 1990. Epidemiology of anther-smut infection of Silene alba caused by Ustilago violacea: patterns of spore deposition and disease incidence. J. Ecol. 78:166-179.

Anderson, R.M and May, R.M. 1979. Population biology of infectious diseases: Part I. Nature 280:361-367.

Andersson, 0 . 1950. The Scanian sand vegetation - A survey. Botaniska Notiser 1950:145-172.

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