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2Institute of Biological Sciences, University of Tsukuba, Tsukuba, Ibaraki 305-8572, Japan; and 4Department of Biology, Faculty of Science, Kyushu University, Fukuoka 812-8581, Japan
Received for publication June 22, 1999. Accepted for publication June 16, 2000.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: Asteraceae • disease ecology • Eupatorium makinoi • extinction • geminivirus • growth • light • population dynamics
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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, research on the roles of pathogens in dynamics and evolutionary responses of natural plant populations has rapidly moved forward. There is an increasing body of evidence showing that fungal pathogens regulate population dynamics of host plants (e.g., Alexander and Antonovics, 1988
; Carlsson and Elmqvist, 1992
; Fowler and Clay, 1995
; Lively et al., 1995
; Wennström, Ericson, and Elveland, 1995
) and also drive evolutionary changes of plant populations (see Clay and Kover, 1996
, for a review). However, a limited number of studies have been done on viral disease in natural habitats (Yahara and Oyama, 1993
; Kelley, 1994
), in spite of the fact that virus infection is a common phenomenon in wild plant populations (MacClement and Richards, 1956
; Raybould et al., 1999
). This is partly because the detection of virus infection requires serological procedures, especially when virus-infected plants do not show visible symptoms. However, advances in molecular biological techniques enable us to detect viruses easily and accurately (e.g., Takahashi et al., 1993
; Ooi et al., 1997
).
Eupatorium makinoi and geminivirus comprise a system suitable for examining ecological and evolutionary consequences of virus infection in natural habitats. First, virus-infected plants can be easily identified because plants express the visible symptom of vein yellowing soon after the infection. The identification by visible symptom is highly reliable and is supported by the fact that no fragments of viral DNA were amplified by PCR (polymerase chain reaction) in isolates from E. makinoi plants without visible symptoms (Ooi et al., 1997
). Secondly, the E. makinoi–geminivirus system poses two interesting issues in relation to coevolutionary processes: the evolution of sex and the mechanism of long-term coexistence of hosts and pathogens. Eupatorium makinoi consists of asexual (agamospermous) and sexual populations, and high incidence of virus infection occurs only in agamospermous populations (Yahara and Oyama, 1993
). Thus, this would be a good model system for testing the Red Queen hypothesis (Hamilton, Axelrod, and Tanese, 1990
; Clay and Kover, 1996
; Lively, 1996
). On the other hand, the oldest record (Eighth century) of a plant virus is that of the geminivirus infecting E. makinoi (Inouye and Osaki, 1980
), which suggests that some mechanisms underlie the long-term coexistence between the asexual host and geminivirus.
In a previous field study on an agamospermous Eupatorium makinoi population, we reported population decline in a shaded habitat within 1 yr after the virus epidemic (Yahara and Oyama, 1993
). However, this 2-yr study was too preliminary to conclude whether this local population would become extinct. Subsequent growth experiments revealed that the performance of infected E. makinoi plants varied largely with growth light environment (Funayama, Hikosaka, and Yahara, 1997
; Funayama and Terashima, 1999
). Virus infection impaired the photosynthetic capacity in E. makinoi leaves (Funayama, Sonoike, and Terashima, 1997
), and shading accelerated the effects of virus infection by reducing photosynthetic production. These results suggest that the population dynamics of E. makinoi plants under virus epidemics could differ with light environment.
In this study, therefore, we conducted long-term observations of the dynamics of agamospermous E. makinoi populations under virus epidemics in two sites with contrasting light environments. We followed the fates of individual plants, because individual-based analyses would lead to a more mechanistic understanding of the population dynamics. The following questions were addressed: (1) What is the consequence of the interaction between E. makinoi and geminivirus in a local region—extinction of both, extinction of the virus, or coexistence? (2) Are the population dynamics under virus epidemics in open habitats different from those in shaded habitats? Based on the data, we discuss mechanisms that enable agamospermous E. makinoi populations to persist for a long time under infection of geminiviruses.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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), and the pathogen was geminivirus (tobacco leaf curl virus, TLCV). Eupatorium makinoi is a perennial consisting of agamospermous and sexual types. In this study, only agamospermous E. makinoi plants were used. Thus, a population is either genetically uniform or composed of a few clonal cytotypes (Watanabe, Furuhara, and Hujiwara, 1982
). In natural habitats, virus-infected plants can be identified by the presence of yellow veins. The virus is transmitted by vectors, two species of whiteflies (Osaki and Inouye, 1979
), but is never transmitted through seeds. Density of whitefly populations in natural habitats is quite low and, thus, it is unlikely that whiteflies themselves affect the growth of E. makinoi plants. Symptoms of virus infection appeared soon after inoculation by grafting (S. Funayama, personal observation). Eupatorium makinoi plants never recover from virus infection. For further biological detail of E. makinoi and the geminivirus, see Funayama, Hikosaka, and Yahara (1997)
, Ooi et al. (1997)
, and Yahara et al. (1998)
.
Study site
Two sites with distinct light environments (Gora-dani, shaded, and Mt. Minou, open) were chosen and plots were set up at each site (Gora-dani, Minou 1, and Minou 2). Gora-dani (33°33' N, 130°34' E, 265 m above sea level) is located in Dazaifu City, Fukuoka Prefecture, Japan. The Gora-dani population was on the floor of a plantation of Japanese cedar, Cryptomeria japonica (L. fil.) D. Don, and the average relative photosynthetic photon flux density (R-PPFD) measured in September at the height of 1.5 m above the ground was 16%. In Gora-dani, Pleioblastus simonii (Carr.) Nakai dominated, and Neolitsea sericea (Bl.) Koidz., Daphniphyllum teijsmannii Zoll. ex Kurz, Rubus hirsutus Thunb., Amphicarpaea edgeworthii Benth. var. japonica Oliver, and Codonopsis lanceolata (Sieb. et Zucc.) Trautv. coexisted. Mt. Minou is in Kurume City, Fukuoka Prefecture, Japan (33°17' N, 130°36' E, 350 m above sea level). Minou 1 and 2 populations were in the clearing for the plantation of Japanese cypress trees, Chamaecyparis obtusa (Sieb. et Zucc.) Endl., and the average R-PPFD level measured in September was 
92% at 1.5 m above the ground in both populations. Saplings of Japanese cypress were 1 m high. Miscanthus sinensis Anderss., Pueraria lobata (Willd.) Ohwi, Solidago altissima L., and Lonicera japonica Thunb. dominated the site. In Mt. Minou, regular mowing was conducted every year in early July.
Demography
In a population at Gora-dani, a 6 x 20 m quadrat was established in 1991 (Yahara and Oyama, 1993
). Demography of the Gora-dani population was studied from 1991 to 1998. For Minou 1 and Minou 2 populations, 7 x 8 m quadrats were established. Demography of the Minou populations was followed from 1994 to 1997. Field census was taken every year in late September or early October except for Minou populations in 1994. In 1994, we took a census of Minou populations in early July.
For all the quadrats, locations of all shoots of E. makinoi, including newly established plants, were mapped, and their infection states were assessed by the disease symptom in leaves (yellowing of the veins). Presence or absence of flowers was also recorded. Newly established plants were identified as the plants that had been absent at the previous census but were present at the current census.
For the Gora-dani population, plant height was measured with a scale. Most plants had only one shoot. Relative stem growth rate (RSGR) was calculated as:
T is 1 yr.
Measurement of PPFD
Photosynthetic photon flux density (PPFD) was measured under diffuse light conditions on densely overcast days in October 1996 using quantum sensors (190SA, LI-COR, Lincoln, Nebraska, USA). For each of the E. makinoi plants, PPFD at the top of the plant and that at the open place were measured simultaneously. Relative PPFD (R-PPFD), the ratio of PPFD at the top of the individual plant to that in the open place, was calculated and used as an index of microsite light availability.
Statistical analyses
The effects of virus infection and of year on plant height in the Gora-dani population were tested with two-way analysis of variance. The effects of virus infection on RSGR in the Gora-dani population were tested with one-way analysis of variance. Post hoc analysis was performed with Dunnett's method. Correlation between plant height and R-PPFD was tested using Fisher's z transformation. To examine the relationship between plant size and mortality or flowering, logistic regression analysis was performed for both infected and uninfected plants in Gora-dani population. Year was treated as a stratum. Data were analyzed with StatView version 5.0 (SAS Institute, Cary, North Carolina, USA) except for logistic regression analysis. Computation of logistic regression analysis was performed with LogXact-Turbo (CYTEL Software Corporation, Cambridge, Massachusetts, USA).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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The proportions of flowering plants in three populations are shown in Fig. 2. In all the populations, the proportion of flowering plants decreased with time.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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This finding agrees well with the expectations from the results of the growth experiments (Funayama, Hikosaka, and Yahara, 1997
; Funayama and Terashima, 1999
) that the population dynamics of E. makinoi plants under a virus epidemic would differ with light environments. Under low-light conditions, impaired photosynthesis in virus-infected leaves caused the negative net production in leaves on cloudy days (Funayama and Terashima, 1999
). Thus, it is highly probable that the photosynthetic production in a whole plant in the shade could be negative in cloudy days and that the integrated yearly carbon gain of infected plants could be negative in shaded habitats. In shaded habitats in the field, infected plants actually showed a negative RSGR (Fig. 4), which indicates poorer regrowth and smaller plant size in the subsequent years. High mortality in infected plants observed under low-light conditions (Funayama, Hikosaka, and Yahara, 1997
) also supports this view. Smaller plants were likely to receive less PPFD due to the shading by surrounding plants and overstory canopy (Fig. 5), which would accelerate the decrease in yearly carbon gain and, finally, cause death.
The above sequence is valid not only for infected plants in Gora-dani, but also for those in Mt. Minou. However, in Minou populations, it took longer for the infected plants to become smaller than the critical size for flowering or survival, because even the small plants received more light due to the absence of the overstory (Fig. 5). Regular mowing conducted on Mt. Minou might also contribute to the long persistence of the populations through preventing the successional changes of vegetation and by keeping the environments bright. In conclusion, dynamics of E. makinoi populations under virus epidemics is well explained by the deterioration of photosynthetic activity of infected leaves and by the characteristics of light environment of the habitats.
The local population of E. makinoi plants in Gora-dani became nearly extinct during this study (Fig. 1a). This result supports the prediction of Alexander and Antonovics (1988)
: if the pathogen is transmitted by insect vectors that search for host plants, high transmission rate of pathogens and low recruitment rate of hosts will cause the local extinction of both host and pathogen populations. In the case of the E. makinoi–geminivirus system, the geminivirus is transmitted by two species of whiteflies that search for limited number of host species, and the efficiency of transmission is quite high (see Fig. 1a, c). Moreover, the dense vegetation cover in Gora-dani made the environment unsuitable for seedling establishment, which resulted in a low recruitment rate (Fig. 1a). Thus, the extinction of this local population in Gora-dani can be explained by high transmission rate and low recruitment rate. However, high transmission rate and low recruitment rate were observed not only in the Gora-dani population, but also in the Minou populations. This suggests that the Minou populations will also become extinct eventually, although population dynamics were apparently different from that in Gora-dani.
Implications for the Red Queen model and the long-term coexistence of the host and virus
Eupatorium makinoi consists of sexual and agamospermous populations and the incidence of virus infection is markedly higher in agamospermous populations (Yahara and Oyama, 1993
). This fact seems to support the Red Queen model, which claims that sexual reproduction is an adaptation against rapidly evolving parasites (Hamilton, Axelrod, and Tanese, 1990
). For the Red Queen model to be applicable, the effects of pathogens must be so severe that the fitness of the sexual plants exceeds that of asexual plants by more than twofold (Clay and Kover, 1996
; Lively, 1996
). Previous short-term work and this study draw the conclusion that geminivirus infection generally extinguishes local agamospermous populations of E. makinoi. This severe impact on the host plants is attributed to the fact that almost all the plants in the population are infected, which is probably due to genetic uniformity of the agamospermous populations (Watanabe, Furuhara, and Hujiwara, 1982
). In contrast, the incidence of geminivirus infection remains quite low in most sexual populations of Eupatorium (Yahara and Oyama, 1993
). This view is supported by the examination of molecular evolution of geminiviruses: when the geminiviruses infecting sexual populations were compared with ones infecting agamospermous populations of Eupatorium, there were significantly more amino acid replacements in the ORF C4 gene, a host range determinant, in geminiviruses isolated from the sexual host populations than in those from the asexual populations (Ooi and Yahara, 1999
). All these findings strongly support relevance of the Red Queen model.
Geminivirus and E. makinoi have coexisted since the Eighth century (Inouye and Osaki, 1980
). The present study, however, indicated the local extinction of E. makinoi populations under virus epidemics. There are two possible mechanisms that enable geminivirus to coexist with their host plants for a long time: one is the existence of alternative hosts. If the alternative hosts exist, geminivirus can persist after the local extinction of E. makinoi populations. Lonicera japonica is known as a wild host of this geminivirus (Osaki, Kobatake, and Inouye, 1979
), and this plant is often observed in the natural habitats of E. makinoi. The second possibility is that E. makinoi coexists with geminivirus in the context of metapopulation dynamics, which is considered to be crucial to understand host–pathogen interactions (Thrall and Burdon, 1997
). It has been proposed that dispersal in space during an essentially pathogen-free phase of the life history may allow the long-term persistence of asexuality despite the considerable effects of their pathogens (Ladle, Johnstone, and Judson, 1993
). As is shown in this study, dynamics of local populations of E. makinoi after virus epidemics varies with light environment in habitats. Since populations in open habitats may persist even when infected by virus, they function as the source of seeds, which causes the establishment of new uninfected populations. Because agamospermous plants of E. makinoi produce many small achenes with pappi, it is probable that the dispersal rate to newly available open places exceeds the dispersal rate of whiteflies. Then, time-delayed dynamics at the metapopulation level will result in long-term coexistence of the hosts and viruses (Tooby, 1982
). Of course, these two mechanisms are not mutually exclusive. Further studies considering both processes are needed to fully understand the coexistence of Eupatorium and geminivirus.
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FOOTNOTES |
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3 Author for correspondence, current address: Department of Biology, Graduate School of Science, Osaka University, Machikaneyama-cho 1-16, Toyonaka, Osaka 560-0043, Japan (Fax +81-6-6850-5808, e-mail: funayama{at}chaos.bio.sci.osaka-u.ac.jp
).
5 Current address: Department of Biology, Graduate School of Science, Osaka University, Machikaneyama-cho 1-16, Toyonaka, Osaka 560-0043, Japan.
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