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Ecology |
Department of Biology, P.O. Box 3000, FIN-90014 University of Oulu, Oulu, Finland
Received for publication June 16, 2006. Accepted for publication May 29, 2007.
ABSTRACT
Climate change may influence the relationship between arctic plants and their symbiotic mycorrhizal fungi. The benefit of the symbiosis for the host plant affects vegetation succession and may be a key parameter in predicting vegetation responses to warming. We investigated the mycorrhizal benefit in the low arctic perennial herbs Potentilla crantzii and Ranunculus acris in symbiosis with the arbuscular mycorrhizal fungus Glomus claroideum. Temperature response in the mycorrhiza-mediated acquisition of nitrogen (N) and phosphorus (P), growth, and photosynthetic nutrient-use efficiency were determined. Near the average natural soil temperature (12°C), mycorrhiza did not improve plant nutrient capture but significantly enhanced plant P capture at 17°C. Photosynthetic nitrogen-use efficiency was higher at 17°C than at 12°C and was further increased by mycorrhiza at 17°C. Photosynthetic phosphorus-use efficiency was not affected by temperature or mycorrhiza. Increasing the growing temperature by 5°C increased the relative shoot growth rate by 15%. Mycorrhizal symbiosis did not enhance plant growth rate, but the plants gained between 20% and 90% more mycorrhiza-mediated P when grown at higher temperature. The results suggest that these low arctic species have good potential to respond positively to increasing temperatures.
Key Words: Arbuscular mycorrhiza • ecophysiology • Glomus claroideum • Potentilla • Ranunculus • symbiotic benefit • warming
Arctic ecosystems are predicted to be among the first systems to be affected by climate change. Predicting the direction and magnitude of the effect of rising temperatures requires better knowledge of the temperature response of arctic organisms. Plant adaptation to the arctic environment is limited by a dilemma: adaptation to colder climate may increase plant nutrient demand, but, at the same time, soil nutrient availability decreases as temperatures decline (Kielland and Chapin, 1992
). The higher nutrient and carbon concentration in cold climate foliage (Chapin, 1980
; Körner, 1989
; Hoch et al., 2002
) suggests that plant metabolism and nutrient relations are fundamentally affected by low temperature. Arctic plants are adapted to grow and function at low growing season temperatures, and their photosynthetic temperature optimum, for instance, is lower than in their temperate relatives (Billings and Mooney, 1968
; Körner and Diemer, 1987
). High N concentration in arctic plant leaves suggests that increasing quantities of enzymes are part of the adaptive mechanism. However, high enzyme production requires more investment into P-rich rRNA, and photosynthesis at lower temperatures requires higher levels of phosphorylated metabolites (Hurry et al., 2000
), suggesting that phosphorus may have a particularly important role in cold climates.
Due to low nutrient availability, mycorrhizal symbiosis and symbiotically mediated nutrient acquisition seem beneficial for the low arctic plants. Most herbaceous plant species form symbiotic relationship with Glomeromycotan fungi in their roots called arbuscular mycorrhiza (AM). Arbuscular mycorrhizal fungi usually improve plant acquisition of nitrogen (Barea et al., 1987
; Hawkins et al., 2000
) and especially phosphorus (Marschner and Dell, 1994
). These two elements frequently limit plant production in arctic and subarctic ecosystems (Shaver and Chapin, 1980
). In addition to providing nutrients, AM may improve plant resistance to root pathogens (Azcón-Aguilar and Barea, 1996
) and increase plant water uptake (Augé, 2001
), which could be particularly important in high latitude ecosystems prone to seasonal drought during their short growing season. In spite of these benefits, high arctic plant species do not generally form a mycorrhizal symbiosis (Bledsoe et al., 1990
; Kohn and Stasovski, 1990
). Low arctic plants are usually colonized, but studies on mycorrhizal functions and host plant benefit in cold climates are few (Ruotsalainen and Kytöviita, 2004
; Kytöviita, 2005
).
Arbuscular mycorrhizal symbionts also affect plant physiology. AM fungi increase plant photosynthate demand as the AM fungi acquire carbon for growth, maintenance, and other metabolic activities from the plant partner. In response, plant photosynthetic activity may increase in AM plants (Eissenstat et al., 1993
; Miller et al., 2002
; Ruotsalainen and Kytöviita, 2004
). The carbon cost of AM symbiosis has varied between 4% and 20% of net photosynthetic gain under laboratory conditions (Paul and Kucey, 1981
; Jakobsen and Rosendahl, 1990
), but may be larger under field conditions where fungal hyphae are constantly consumed by soil fungivores. Despite considerable carbon costs, it is generally thought that association with mycorrhizal fungi benefits the plants, usually in the form of improved nutritional status and growth. Low temperature and associated low nutrient availability also favor plant carbon allocation to belowground structures, such as rhizomes or large fine root systems (Chapin, 1980
; Körner and Renhardt, 1987
). However, the effect of low temperatures on host plant carbon allocation to mycorrhizal symbionts and on the host plant mycorrhizal benefit is not known. The predicted warming of cold climate areas can affect vegetation directly, but also indirectly via effects on soil microbes (Jonasson et al., 2001
). If plants and mycorrhizal fungi respond differently to increasing temperature, then a change in mycorrhizal benefit can be expected. Because mycorrhizal benefit is one of the factors affecting plant coexistence and vegetation succession (Allen, 1991
), it is one of the key parameters in predicting vegetation responses to warming.
The aim of the present experiment was to test the potential of two low arctic herbs and their mycorrhizal associate to respond to warming. Specifically, we hypothesized that if low arctic plants and their mycorrhizal symbionts are both adapted to cold climate, the plants should gain some mycorrhizal benefit at the relatively low ambient temperature. Furthermore, we hypothesized that if the plant and the symbiotic fungal performance are symmetric under fluctuating temperature, increasing temperature by 5°C should not affect mycorrhizal benefit to the plant.
MATERIALS AND METHODS
In a factorial climate chamber experiment, adult, low-arctic meadow plants were grown with (MI = mycorrhiza-inoculated) or without (NI = noninoculated) an arbuscular mycorrhizal fungus at two temperatures: prevailing top soil temperature of the site of origin of the experimental organisms (12°C) and 5°C higher (17°C). Plant photosynthesis, nitrogen and phosphorus contents, and fungal colonization intensity were determined after 7–8 wk.
Study organisms
Potentilla crantzii (Crantz) Beck ex Fritsch is an amphiatlantic species that occurs in northern Canada, Greenland, Scandinavia, and the alpine regions of Europe (Hultén, 1958
). Ranunculus acris (Regel) is a circumpolar species. Both species are geographically variable. The seeds were collected from a low arctic meadow at Kilpisjärvi, Finnish Lapland (69°03' N, 20°50' E), that has a snow-free period lasting c. 3 mo. The geographical races of Potentilla crantzii are not described, but the plants of Ranunculus acris used in the present work belong to the subspecies pumilus, which has a Eurasian arctic distribution (Hultén, 1970
). Both P. crantzii and R. acris are common in low arctic meadows, i.e., at the site of seed origin, they were among the six most common herbs. The fungal isolate used, Glomus claroideum, was originally isolated from a subarctic field at Muddusjärvi, in northern Finland (69°8' N, 27°6' E). The global distribution of arbuscular mycorrhizal fungi is not described, but G. claroideum has been isolated from North and South America, Europe, and India (Walker and Vestberg, 1998
).
Pregrowing the organisms
The seeds were collected in September 1999 and placed into moist heat-sterilized sand in perforated aluminum foil packets in January 2000 and stratified at 4°C for 14 mo. Subsequently, the seedlings were grown in a greenhouse for 1 mo and replanted individually into larger pots containing heat-sterilized sand; they were watered with tap water and dilute additions of Ingestad nutrient solution (Ingestad, 1979
). In September 2001, the plants were transferred to climatic chambers set to 8°C to vernalize the plants. During this time, the pots were watered with tap water only, and the light period was gradually changed from 20 h light, 4 h darkness to 12 h + 12 h.
Experimental conditions
In the beginning of April 2002, the 1-yr-old plants were transferred into pots filled with 400 cm2 of a 5:1 mixture of sterile sand and sieved unfertilized, nonsterile peat with 5 g dolomite, 1.5 g/L bone meal (Biolan Biolan Oy, Kauttua, Finland). Bone meal is a slow-release organic fertilizer, whereas peat increases the organic matter content and carries natural soil microbes to the pots but does not contain AM fungal propagules. The substrate pH was 5.6, and total initial P and N were 182 and 119 µg·g–1. The substrate mixture was prepared 1 wk before the potting. There was one plant per pot and 52 and 48 plants of Potentilla and Ranunculus, respectively. Half of these were assigned to the mycorrhiza-inoculation (MI) treatment and were inoculated with about 300 spores of Glomus claroideum in 3 mL of water. The spores had been propagated under laboratory conditions in symbiosis with Sibbaldia procumbens, another low arctic herb. The remaining half of the plants were assigned to the noninoculated (NI) treatment and received 3 mL of sieved (53 µm) spore-free water of the inoculum.
After inoculation and potting, the MI and NI plants were randomly assigned into two separate climatic chambers set to either 12°C or 17°C. The average July–August 2001–2004 top-soil temperature at the site of origin of the seed material was 10.6°C (M.-M. Kytöviita, unpublished data), and therefore we chose 12°C as a good average natural soil temperature to which the organisms should have been adapted. On the other hand, although markedly higher, 17°C is not an unnaturally high soil temperature at these sites. The light period was 20 h light/4 h darkness, and relative air humidity was 40% in both temperature regimes. The amount of light at the plant shoot was about 500 µmol·m–2·s–1, provided by 400 W sodium pressure lamps (OSRAM HQI, Osram, Porvoo, Finland). During the 4-h dark period, dim light was provided by 60W standard light bulbs to simulate polar day conditions that prevail in the original habitat of the organisms during the summer. The temperature treatments and plants were switched between the two chambers every 2 wk to avoid potential differences in the chamber environment other than temperature affecting the plants differently. The plants were watered with tap water about three times per week to keep the substrate moist. Both species flower in their natural habitat within 6 wk after snowmelt. During the experimental 7–8 wk period, 2–5 plants in each treatment category started flowering. The phenology of the plants as indicated by flowering frequency was not affected by either mycorrhizal inoculation or temperature, and the flowering data are not reported further.
Photosynthesis measurements
Photosynthesis in Ranunculus and Potentilla shoots was measured after 7 and 8 wk in the growth chambers, respectively, using LiCor 6400 portable photosynthesis measurement system equipped with a 1-L chamber (LiCor, Lincoln, Nebraska, USA). The whole plant shoot was enclosed in the chamber and gas exchange followed until a stable reading was obtained. A reading was considered stable if continuously monitored chamber CO2 concentration varied less than 1% during 1 min. All measurements were conducted in systematic order in blocks of four containing one replicate of each of the four treatments (NI 12°C, MI 12°C, NI 17°C, MI 17°C).
Plant biomass and fungal colonization
After photosynthesis was measured, the shoot was cut off, scanned to determine the surface area, and dried in an oven at 80°C overnight. The roots were carefully washed clean of the substrate, and a 15-cm sample from different root parts of each plant specimen was taken for fungal colonization analyses. Fungal colonization of roots (calculated both as arbuscular and hyphal colonization) was assessed using the trypan blue staining method of Phillips and Hayman (1970)
, and the gridline–intersection method of McGonigle et al. (1990)
. Ten plants of both species were dried at the time of inoculation; these provided the initial biomass values. Relative growth rate (RGR) was calculated as (ln shoot mass in the end of the experiment- ln shoot mass in start)/number of days in the experiment.
N and P analyses
Shoot N concentration ([N]) was analyzed using the dynamic flash combustion technique (CE Instruments EA 1110 Elemental Analyzers, Wigan, UK). Analysis of P concentration ([P]) in plant shoots was modified from procedure described by John (1970)
. Dried and milled plant tissue was acid digested using the Paar001H program in the Paar Physica multiwave sample preparation system (Perkin Elmer, Waltham, Massachusetts, USA). P concentration was measured as absorbance at 882 nm (UV-160A Shimadzu, Duisburg, Germany). Selected samples gave identical P concentrations when determined in this manner and when determined by HCl extraction of ashed samples followed by plasma emission spectroscopy by Novalab Oy (Karkkila, Finland).
Calculated variables
Photosynthetic N and P use efficiency (PNUE and PPUE) were calculated as the photosynthetic rate divided by leaf N or leaf P concentration on a leaf area basis. Plant mycorrhizal growth benefit was calculated as the ratio of plant RGR between MI and NI plants (MI/NI). Similarly, plant mycorrhizal nutrient benefit is expressed as the ratio of concentration or plant total N or P between MI and NI plants.
Statistical analyses
Several variables were measured from each plant. To avoid risks associated with repeatedly measuring the same plants, multivariate analyses of variance (MANOVA) were conducted on the data. Conventional ANOVA was also performed; ANOVA conducted separately on each variable and MANOVA gave similar results. The three factors in overall MANOVA (plant species, temperature, and inoculation) and in two-factor MANOVA conducted per plant species had significant main effects as well as interactions. The two plant species were further analyzed separately in two-factor ANOVA to elucidate which variables contributed significantly to the overall effects. When there were significant interactions between the temperature and inoculation treatments, a one-factor ANOVA was conducted followed by Tukey's test. Multivariate normality was assumed when each dependent variate showed univariate normality according to Kolmogorov–Smirnov's test. In Potentilla, data for milligrams N per shoot were not normally distributed. The assumption of equal covariance was not met, and therefore Pillai's Trace was chosen as the test statistic because it has been shown to be robust against departures from covariance equality (Zar, 1999
; Scheiner, 2001
). Mycorrhizal colonization was variable and was not detected in all inoculated plants. To elucidate whether physiological effects depended on colonization, we performed one-factor MANCOVA analyses for all inoculated plants with colonization intensity as a covariate and temperature as the independent factor. Differences in mycorrhizal colonization rates at the two temperatures were assessed with one-factor ANOVA conducted separately for the two species. Statistical analyses were performed using SPSS software, version 14.0 (SPSS Inc., Chicago, Illinois, USA).
RESULTS
Photosynthesis and growth
Mycorrhizal inoculation did not increase photosynthetic rates in either plant species, whereas Ranunculus had consistently higher photosynthetic rates than Potentilla (Tables 1 and 2). Despite no marked effects of temperature on net photosynthesis, plant shoot RGR was significantly higher at 17°C than at 12°C (Tables 1 and 2). Mycorrhizal inoculation did not affect shoot RGR (Tables 1 and 2). Root RGR was similarly increased by increased temperature (Tables 1 and 2). In Ranunculus, inoculation significantly reduced the root RGR (Tables 1 and 2).
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Mycorrhizal colonization intensity
Mycorrhizal colonization was observed in 50% of the MI plants at 12°C, and in all MI plants at 17°C. Both arbuscular and hyphal colonization rates were significantly lower at 12°C both in Ranunculus (arbuscular: F1,21 = 17.159, P < 0.001; hyphal: F1,21 = 37.07, P < 0.001) and Potentilla (arbuscular: F1,25 = 8.74, P = 0.007; hyphal: F1,25 = 11.63, P = 0.002) (Fig. 1). No mycorrhizal structures were observed in NI plants. The overall effect of temperature in MANCOVA was significant for both species (Potentilla: Pillai's Trace = 0.867, F8,15 = 12.171, P < 0.001, Ranunculus: Pillai's Trace = 0.740, F8,10 = 3.60, P = 0.03), but the effect of colonization intensity as a covariate was not significant (Potentilla: Pillai's Trace = 0.387, F8,15 = 1.18, P = 0.370, Ranunculus: Pillai's Trace = 0.377, F8,10 = 0.756, P = 0.647), despite relatively variable colonization rates.
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Arctic ecosystems have distinctively low soil nutrient availability, a characteristic which generally favors mycorrhizal development and mycorrhiza-mediated nutrient uptake. In the present work, we examined mycorrhizal benefit in the low arctic Potentilla crantzii and Ranunculus acris in terms of plant growth and nutrient acquisition at two temperatures. Our experiment simulated the ecological conditions in the original habitat where the growing season is short and relatively cold and where early onset of growth and nutrient uptake are important. Therefore, because we assumed the plants and the fungus to be adapted to low growing-season temperatures, we expected mycorrhizal benefit at 12°C, which is close to the natural average top soil temperature. However, neither species grew better or gained more nutrients at 12°C, despite moderate colonization rate by the arbuscular mycorrhizal fungus Glomus claroideum. This result is surprising because both species support abundant AM colonization under field conditions (Ruotsalainen et al., 2002
; M.-M. Kytöviita2 and A. L. Ruotsalainen, personal observations) with an average growing-season top-soil temperature of 10.6°C. The experimental conditions were designed to favor mycorrhizal formation, and when the identical substrate with higher temperatures was used, the present fungal strain benefited several low arctic plant species (Kytöviita et al., 2003
; Ruotsalainen and Kytöviita, 2004
), as was also the case at the higher temperature regime in the present experiment. If mycorrhizal symbiosis is important to plant performance in cold climate, some mycorrhizal benefit should be manifested under the prevailing temperature regimes of cold climate areas. It is possible, although not evident in the present experiment, that plants may still benefit from mycorrhizae under natural conditions because the improvement may not be predominantly in growth or nutrient gain, but in increased water acquisition and protection against root herbivores or root pathogens (Azcón-Aguilar and Barea, 1996
; Augé, 2001
).
Mycorrhiza-mediated nutrient acquisition in the cold may be low because it is restricted by the inability of the AM fungus to function at low temperatures. AM fungi may require a relatively high temperature to be fully functional, and the optimum temperature for mycorrhizal functions may be as high as 25°C with little adaptation by arctic strains (Kytöviita, 2005
). Very few studies have investigated the effects of temperature on the functioning of AM fungi, but the available evidence indicates that even moderately low temperature (10–12°C) limits hyphal growth (Heinemeyer and Fitter, 2004
; Gavito et al., 2005
) and that AM hyphae are unable to absorb P at 0°C (Wang et al., 2002
). This is in contrast to arctic plants, which can grow at 10°C and absorb nutrients at temperatures close to 0°C (Chapin and Bloom, 1976
; Müllen et al., 1998
). Nutrient absorption and/or transfer in the plant may require higher temperatures than does the consumption of plant carbon. This could explain why in some cases the mycorrhizae actually reduced growth at low temperatures (i.e., the fungi acted parasitically in cold [Hayman, 1974
]) and how plants could be colonized in cold climate ecosystems without nutrient or growth benefit to the plant. In the present experiment, it is evident that the AM fungus was able to germinate and acquire C from the plant to the extent that it moderately colonized the plant roots at 12°C. However, there was no evidence for a fully functional mutualism in terms of mycorrhiza-mediated nutrient acquisition by the plants at 12°C.
The present results suggest that increasing temperature increases mycorrhizal benefit in mycotrophic low arctic plants: mycorrhizal plants gained markedly mycorrhiza-mediated nutrients at 17°C, but not at 12°C. Previous research has shown that increasing temperatures from 14°C to 20°C increases the mycorrhizal benefit in the temperate Allium and Gossypium plants (Furlan and Fortin, 1973
; Hayman, 1974
; Smith and Roncadori, 1986
). Similarly, increasing temperatures from 8°C to 15°C increased the mycorrhizal benefit in the low arctic Gnaphalium seedlings (Ruotsalainen and Kytöviita, 2004
). The increase in mycorrhizal benefit at higher temperature indicates that AM fungi and their host plants do not respond to increasing temperature symmetrically. Both Potentilla and Ranunculus responded positively to warming. Increasing the growing temperature by 5°C increased the shoot RGR in these low arctic herbs by 15% on average. Increasing temperature also increased the root RGR; in noninoculated plants the increase in root RGR was 41% in Potentilla and 32% in Ranunculus. However, the 5°C increase in temperature greatly increased the relative frequency of mycorrhizal structures in plant roots by 50% and 400% in Potentilla and Ranunculus, respectively. Therefore, although both the fungus and plant benefit from warmer temperatures (Baon et al., 1994
; Smith and Roncadori, 1994; Ruotsalainen and Kytöviita, 2004
), the 5°C increase in temperature in the current study benefited the fungus much more than the plant. Higher colonization intensity and higher mycorrhizal benefit in Ranunculus indicate that this species may be more mycotrophic than Potentilla and suggests that not only may Ranunculus allocate more C to mycorrhizal functions, but it may also gain more benefit in return. Frequency of arbuscules, the putative sites of nutrient transfer, was moderate, indicating potential for functional symbiosis and resource exchange in all cases. Even low colonization rates (less than 20% root length colonized) may cause the plant to gain nutrient benefit from the symbiosis (Sanders and Koide, 1994
; Wilson and Hartnett, 1998
).
Higher [N] and high N allocation to photosynthetic proteins in cold climate plants (Berry and Björkman, 1980
) is an adaptation to low temperature. Although this adaptation enables high photosynthetic rates even when low temperatures reduce enzyme activity, it leads to lower PNUE at lower temperature. This is evident also in the present work. Decreasing PNUE is predicted to reduce plant C allocation to root symbionts and result in lower mycorrhizal colonization (Tuomi et al., 2001
). Thus, the lower mycorrhizal colonization intensity at 12°C could theoretically be explained by the lower PNUE at 12°C. Alternatively, the fungus may not have been fully functional at 12°C, and therefore low colonization did not result from low PNUE. Mycorrhizal symbiosis did not increase plant N capture in the present work, although AM frequently enhance plant N acquisition (Barea et al., 1987
; Ruotsalainen and Kytöviita, 2004
). However, mycorrhizal colonization increased PNUE at 17°C as previously shown for the low arctic herb Gnaphalium (Ruotsalainen and Kytöviita, 2004
). Higher PNUE in mycorrhizal plants at 17°C could be associated with mycorrhizae reducing the sink limitation on photosynthesis. Mycorrhizal symbiosis is frequently associated with enhanced host photosynthetic rates, which is thought to arise from enhanced sink for carbon in the roots (Douds et al., 1988
; Wright et al., 1998
). If the mycorrhiza-induced increase in photosynthesis is not associated with an increase in nutrient concentration of similar magnitude, mycorrhizal colonization may increase photosynthetic nutrient use efficiency as has been shown for PPUE in barley even at low colonization levels (Fay et al., 1996
). Furthermore, mycorrhizas could enhance photosynthetic rates by increasing shoot [P] (Allen et al., 1981
), which does not necessarily result in a change in PPUE. In the present experiment, mycorrhizal inoculation or colonization intensity did not affect plant photosynthetic rates or PPUE, despite the higher [P] in MI plants at 17°C. This indicates a remarkable stability of PPUE across widely different [P]. Photosynthetic rates were not directly associated with RGR, indicating that factors other than carbon are important for limiting plant growth in cold climates, as has been previously suggested for alpine systems (Diemer and Körner, 1996
; Hoch et al., 2002
; Körner, 2003
).
Altogether, mycorrhizal performance improved with increased temperature, and the plants gained between 20% and 90% (Potentilla and Ranunculus, respectively) more mycorrhiza-mediated P at 17°C than at 12°C. Although higher mycorrhiza-mediated P acquisition was not associated with improved RGR, it may still be an important component of plant fitness, because higher mycorrhiza-mediated plant [P] may improve the offspring quality (Nuortila et al., 2004
). Furthermore, warming has been shown to increase seed number in alpine Ranunculus acris (Tøtland, 1999
). Therefore, increased mycorrhiza-mediated nutrient uptake induced by environmental warming may improve seedling recruitment of cold climate meadow plants and thus support population persistence. Further evaluation of the impact of global warming on arctic ecosystems should include studies on different cold climate plant species and AM fungi as well as studies on the invasibility of temperate species into low arctic plant and fungal communities.
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1 The authors thank T. Pakonen and T. Törmänen for technical and laboratory assistance and M. Weih for useful discussions. This study was financed by Academy of Finland (M.-M. K.) and the Cultural Foundation of Northern Savo (A.L.R.). 
2 Author for correspondence (minna-maarit.kytoviita{at}oulu.fi
)
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) and arbuscules (
) in (a) Potentilla crantzii, and (b) Ranunculus acris grown at 12°C and at 17°C