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ABSTRACT |
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Pisolithus is restricted in New Zealand to geothermal areas where it associates with Kunzea ericoides var. microflora (prostrate kanuka) and occasionally Leptospermum scoparium. Here we describe for the first time the ectomycorrhizal morphotypes of three New Zealand Pisolithus species and report the frequency and abundance of these morphotypes against other mycorrhizal fungi associated with these hosts in New Zealand geothermal areas. The three Pisolithus species form typical ectomycorrhizal associations with Kunzea ericoides var. microflora, and one also was observed forming typical ectomycorrhizal associations with Leptospermum scoparium. Although the morphotypes from the three Pisolithus species share many morphological and anatomical characteristics, they vary with regard to the abundance of rhizomorphs. The common occurrence of Pisolithus fruiting bodies at the geothermal sites was matched by frequent and abundant Pisolithus ectomycorrhizas. Pisolithus ectomycorrhizas were frequent (100% of soil cores) and abundant (between 55 and 88% of ectomycorrhizal tips) associates of prostrate kanuka in hot (50 C at 8 cm depth), highly acidic and N depleted soils. The levels of arbuscular mycorrhizal colonization of prostrate kanuka were lower than on K. ericoides and L. scoparium on cooler soils. The stressful conditions where prostrate kanuka dominates probably favor Pisolithus over the mycorrhizal fungi occurring in cooler geothermal areas. Questions about how several genetically similar Pisolithus species co-occur on prostrate kanuka in geothermal areas without mutual competitive exclusion are discussed.
Key words: arbuscular mycorrhizas, ectomycorrhizas, geothermal, Kunzea ericoides var. microflora, New Zealand, Pisolithus
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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) and forms ectomycorrhizal (EcM) associations with a broad range of woody plants including members of Myrtaceae, Mimosaceae, Pinaceae, Fagaceae, Cistaceae, Dipterocarpaceae and Caesalpiniaceae. It has been recorded in a range of environments including forests and plantation sites, eroded soils and mining sites (Gardner and Malajczuk 1988), and along road margins (Marx 1977). Isolates of Pisolithus are some of the most commonly used in forestry, with growth stimulation reported for several tree species including eucalypts, pines and acacias (Garbaye et al 1988, Marx et al 1977, Duponnois and Ba 1999). Pisolithus has proved particularly effective in improving plant growth on drier soils with high soil temperature (Momoh and Gbadegesign 1980, Marx et al 1985), and isolates of this fungus also alleviated Al sensitivity in Pinus (Cumming and Weinstein 1990).
The common presence of Pisolithus fruit bodies in New Zealand (NZ) geothermal areas suggests this fungal genus is an important EcM associate of Leptospermoideae in these particular ecosystems. However, molecular studies comparing above- and below-ground views of fungal dominance in several genera other than Pisolithus have revealed that few fungal species show consistent correspondence between above- and below-ground abundance (Horton and Bruns 2001). Correlation between fruit body presence and EcM of the same species or genet at a local level has been demonstrated only for a limited number of species including Paxillus involutus (Laiho 1970), Hebeloma cylindrosporum (Guidot et al 2001) and Suillus grevillei (Zhou et al 2001). A study of Pisolithus EcM abundance therefore is needed to evaluate the ecological importance of this EcM fungus in New Zealand geothermal areas.
Pisolithus is restricted in NZ to geothermal areas, where it associates with Kunzea ericoides var. microflora (prostrate kanuka). A recent study (Moyersoen et al 2003) reported three Pisolithus phylogenetic clades in New Zealand, matching the species P. marmoratus, P. albus and an unnamed taxon P. species 10, that occur naturally in Australia. These three species were recorded from the same geothermal site, and two species were found on prostrate kanuka root tips in the same soil volume (Moyersoen et al 2003).
To our knowledge, the presence of Pisolithus in geothermal areas outside NZ has been reported only in Yellowstone National Park (Cullings and Makhija 2001). Although Pisolithus fruit bodies were common in Yellowstone geothermal areas, Cullings and Makhija (2001) failed to observe Pisolithus EcM in the same areas and these authors questioned the importance of this fungus as an EcM associate of Pinus contorta.
In this study, we report variations in the habit of EcM morphotypes belonging to the three Pisolithus species in New Zealand geothermal areas. The quantification of these Pisolithus morphotypes let us confirm the abundance of Pisolithus EcM in the active geothermal areas where prostrate kanuka dominates.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). EcM were identified using ITS-RFLP as described by Moyersoen et al (2003). The location of sampling sites is described in Moyersoen et al (2003). Fixed specimens are stored in the University of Liège Herbarium (LG).
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), and two subsamples belonging to the same mycorrhizal cluster were stored either in water or fixed in formaldehydeethanol(70%)-acetic acid (5:90:5) (FEA) or glycerol-ethanol-H2O (1:1:1) for further anatomical description. Within 24 h of collection, the habit of EcM subsamples stored in water was recorded with a dissecting microscope fitted with a digital camera. Automontage V 1 software (Synoptics Ltd, Cambridge, UK) was used to enhance field depth. The anatomical features of EcM were described from mantle peels using Agerer’s (1991) method of description. Root sections of selected EcM material were performed by cryotomy for further description of Hartig net anatomy.
Mycorrhiza scoring. –
Three randomly located soil cores were taken from four geothermal sites: Tokaanu, Tauhara, Karapiti and Te Kopia. The location of these sites is described in Moyersoen et al (2003). At Te Kopia two vegetation types were recognized and three soil cores were taken from each vegetation type. The soil cores were approximately 10 x 10 x 10 cm and included the surface organic soil horizon where the density of fine roots was greatest. The depth of organic soil was recorded and surrounding vegetation characterized for each core. Surface (2 cm depth) and deeper (8 cm) soil temperatures were recorded in the field before removal of the soil core. Soil samples were stored at 5 C before further root processing and soil chemical analysis. Each soil core was subdivided into two soil subsamples. Roots were washed from the soil in one subsample, and fine roots of K. ericoides and/or L. scoparium were extracted. Total fine root length of these species was measured using Tennant’s (1975) modified line intercept method. Pisolithus EcM tips were identified on the basis of their habit and anatomy (Weiss 1992, Watling et al 1995, this study) and scored against other EcM morphotypes and noninfected root tips using Hatch’s (1937) method. After EcM scoring, the fine roots were cut into approximately 1 cm long pieces and a subsample of approximately 100 cm was selected randomly for further arbuscular mycorrhizas (AM) scoring. These root pieces were cleared and stained using a phenolfree modification of the method of Phillips and Hayman (1970). Arbuscular mycorrhizas were scored following McGonigle et al (1990) with a compound microscope, 200x magnification. Arbuscules, vesicles and hyphal coils were recognized as diagnostic for AM. One slide was screened per sample, with a range of 19–61 root pieces screened per slide. Chemical analysis of the remaining soil subsamples included pH (measured in water), KCl extractable Al, %C and %N (ignition method), and Olsen extractable P.
Statistical analysis. – To meet the assumption of the normal distribution, mycorrhizal fractional colonization data were arcsin transformed before further analysis. For simplicity, the five sampling locations were grouped in the two vegetation categories: mixed shrubland (Tokaanu, Te Kopia 2) and prostrate kanuka vegetation (Tauhara, Karapiti, Te Kopia 1). Mean soil parameters and mycorrhizal fractional colonization values were measured for each sampling location, and the effects of vegetation category in soil chemical characteristics and mycorrhizal fractional colonization were determined on these mean values in a t-test (Systat version 7.0).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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), one of them (RFLP type A, P. species 10) was observed both on K. ericoides var. microflora and L. scoparium. The three remaining RFLP patterns belonging to P. marmoratus (RFLP D), P. albus (RFLP B) and P. species 10 (RFLP C) were observed only on K. ericoides var. microflora.
The ectomycorrhizal system of all four RFLP types was monopodial pinnate and tended to form clusters under fruit bodies. The color was whitish or yellow orange (FIG. 1A–D). The surface was smooth, hydrophobic, and covered with a veil of emanating hyphae. The rhizomorphs either were infrequent or abundant and occurred throughout the mycorrhizal system; they were compact, frequently branched and reached at least 1 cm in length. The single RFLP type D specimen (FIG. 1A) was white and presented fewer rhizomorphs than types A, B and C specimens (FIG. 1B–D). RFLP types A, B and C EcM were often yellow-orange.
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). The hyphal mantle of the four EcM RFLP types was plectenchymatous, with no recognizable pattern in the organization (FIG. 1F) and more densely arranged in deeper layers than in the outer layer. Hyphae with clamp connections were observed across the entire mantle; they were ramified and with short, open anastomoses (FIG. 1E). Hyphal cells in the outer mantle layer often had colorless or yellow contents, and the surface often was covered with yellow or brownish deposits in yellow-colored EcM specimens. The rhizomorphs (FIG. 1G) were either thin (9–25 µm diam) or thicker (60–150 µm), with tightly interwoven hyphae. The diameter of hyphae in the rhizomorphs increased centripetally. Vessel hyphae (FIG. 1G) with thicker diameter and thicker walls, clamp connections or partially dissolved septa were distributed either in the center or randomly in the rhizomorphs. The mantle longitudinal section (FIG. 1H) was 35–50 µm thick and composed of a loosely arranged outer layer and a denser inner layer. The Hartig net was incomplete (FIG. 1H) or paraepidermic.
Pisolithus ectomycorrhizal colonization in relation with vegetation types. –
Two vegetation categories were recognized on the basis of vegetation structure in the four geothermal sites where soil cores were taken. The vegetation at Tokaanu was characterized by a mixed shrubland with canopy up to 6 m composed of a mixture of the two EcM plant hosts L. scoparium and K. ericoides, together with nonectomycorrhizal plant species. Vegetation at Tauhara, Karapiti and Te Kopia (Te Kopia 1 in TABLES II and III) belonged to prostrate kanuka type. Prostrate kanuka vegetation where soil cores were collected at Tauhara and Te Kopia 1 was similar to the description of association D by Burns (1997). Cores at Karapiti were collected in a prostrate kanuka vegetation type similar to a transition between zones 3 and 4 described by Given (1980). A second set of three cores also was collected in Te Kopia (Te Kopia 2 in TABLES II and III) in a mixed shrubland similar to association B described by Burns (1997), with canopy up to 3 m dominated by L. scoparium and the nonectomycorrhizal plant species Weinmannia racemosa.
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). Average soil temperature of 50 C at 8 cm in prostrate kanuka vegetation is within the range of soil temperatures measured at similar depth by other researchers in the same kind of vegetation (Given 1980, Burns 1997). This temperature was significantly higher than mean temperature in mixed shrubland (22.5 C) of Tokaanu and Te Kopia 2 (t3 = –3.631, P = 0.036). The organic horizon layer where cores were taken tended to be of greater depth in mixed shrubland than in prostrate kanuka vegetation on the most geothermally active areas (Karapiti, Te Kopia 1) and the difference between prostrate kanuka vegetation and mixed shrubland was significant at P <0.1 (t3 = 3.027, P = 0.056). Soil C contents were high in mixed shrubland and tended to be lower in prostrate kanuka vegetation, although this trend was not statistically significant (t2 = 1.619, P = 0.247). Vegetation was sparse in Karapiti, and K. ericoides var microflora roots were superficial above the mineral soil in a thin organic layer colonized by mosses and liverworts. High C/N ratios and low total N are consistent with soil N depletion in geothermal areas (Given 1980, Burns 1997). As a consequence of extreme acidity, extractable Al levels were high (Tokaanu) or very high (Tauhara, Te Kopia 1). Medium levels of extractable Al were observed in the less acidic soil of Te Kopia 2 mixed shrubland. Extractable P levels were generally low in our sites. High levels of Olsen P in Tauhara demonstrate that P availability varies in geothermal soils. Several factors might lead to high levels of extractable P in Tauhara. These factors include: extreme acidity leading to solubility of P and high temperature leading to P release from mineral soils.
Total fine root length screened for EcM in each soil core varied between 53 and 610 cm. Average overall EcM colonization in soil cores from mixed shrubland (34%) and prostrate kanuka vegetation (43%) was statistically similar (t3 = 0.715, P = 0.526). Pisolithus EcM dominated the EcM fungal community in prostrate kanuka vegetation only. None of the soil cores sampled in mixed shrubland contained Pisolithus EcM morphotypes, whereas 100% of soil cores from prostrate kanuka vegetation were colonized by Pisolithus morphotypes. Pisolithus EcM colonization was greater than colonization by other fungi in prostrate kanuka vegetation (TABLE III), and the difference of colonization between the two categories of fungi was significant at P <0.1 (t4 = –2.600, P = 0.060). The average abundance of Pisolithus EcM tips relative to total number of EcM tips in roots of prostrate kanuka was 55, 86 and 88% in Te Kopia 1, Karapiti and Tauhara sites, respectively.
Fine root length not colonized by EcM was colonized by AM to different levels (TABLE III). AM were observed in roots of prostrate kanuka, although levels of colonization were significantly lower in prostrate kanuka vegetation (t3 = –4.970, P = 0.016) than in mixed shrubland (TABLE III).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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findings about the natural occurrence of Pisolithus in geothermal soils where a compatible EcM host is present. Pisolithus was a common fruit body genus in Yellowstone’s geothermal areas (Cullings and Makhija 2001), but these authors failed to observe Pisolithus EcM on Pinus contorta roots. In contrast, in most active geothermal areas of our sites Pisolithus dominated the EcM fungus community associated with K. ericoides var. microflora roots. Few detailed descriptions of Pisolithus EcM are found in the literature, and the species involved were identified as P. tinctorius (Weiss 1992, Massicotte et al 1987) and P. aurantioscabrosus Watling (Watling et al 1995). EcM of P. marmoratus, P. albus and P. species 10, described for the first time in our study, had a distinctive habit (color whitish to yellow orange with smooth, hydrophobic mantle covered by a veil of emanating hyphae, and compact rhizomorphs either rare or frequent) and anatomical characteristics (plectenchymatous mantle of ramified hyphae with clamp connections and short open anastomoses and rhizomorphs with tightly interwoven hyphae and either central or randomly distributed vessel-like hyphae). They were distinguished easily from other EcM morphotypes belonging to other fungus species in the same area. The absence of Pisolithus EcM in soil cores in Tokaanu, where species 10 fruit bodies have been collected (Moyersoen et al 2003), is interpreted as an overall scarceness of Pisolithus in less active geothermal areas and the independent sampling of root and fruit bodies. Cullings and Makhija (2001) explained the lack of Pisolithus EcM in Yellowstone by the capacity of this fungus to obtain carbon saprophytically in thermal areas. In contrast, our results demonstrate that three Pisolithus species form typical EcM associations with K. ericoides var microflora in NZ geothermal areas.
The restriction of the dominance of Pisolithus EcM to prostrate kanuka suggests the particularly harsh edaphic conditions characteristic of this vegetation type also favor the presence of these fungi. Levels of EcM colonization similar to the ones observed on K. ericoides var. microflora and involving fungi other than Pisolithus were observed on L. scoparium in adjacent mixed vegetation in cooler geothermal soils of Te Kopia 2. This trend might be explained by host specificity of the three NZ Pisolithus species with K. ericoides var. microflora. However, the association of P. species 10 with L. scoparium in Kuirau Park and the observation of fruit bodies of this species in Tokaanu mixed vegetation where L. scoparium and K. ericoides codominated (Moyersoen et al 2003) showed that species 10 is capable of associating with different Leptospermoideae along the geothermal gradient. The common association of P. marmoratus, P. albus and P. species 10 with eucalypts in Australia (Martin et al 2002, Anderson et al 2001) further demonstrates the capacity of these Pisolithus species to associate with a broad range of Leptospermoideae. The dominance of these three fungal species in prostrate kanuka vegetation is more likely related to a combination of circumstances including the presence of a compatible EcM plant host in active geothermal areas and the autecology of Pisolithus. Pisolithus is considered in Australia and elsewhere as stress tolerant and a poor competitor with other EcM fungi (Cairney and Chambers 1997). This genus was one of the early colonizers of mine sites characterized by warm temperature and poorly developed litter layer, and no fruit bodies were observed in eucalypt forests in the same area (Gardner and Malajzuk 1988). Marx et al (1970) reported the growth response of Pisolithus tinctorius mycelium to temperature, and Marx and Bryan (1971) showed that Pisolithus tinctorius colonization improves plant survival at temperatures up to 40 C. The particularly harsh edaphic conditions where K. ericoides var. microflora dominates probably favor the presence of the stress-tolerant Pisolithus against other EcM fungi present in cooler soils in the same geothermal areas.
Cullings and Makhija (2001) said that several EcM fungus species in addition to Pisolithus species are adapted to extreme edaphic conditions in Yellow-stone thermal areas. Although we observed a dominance of Pisolithus EcM under the most stressful edaphic conditions, other morphotypes also were present. An unidentified species of Scleroderma was observed fruiting abundantly in Te Kopia and Lake Rotokawa prostrate kanuka vegetation (unpublished data) and indicates this mycorrhizal fungus probably associates with K. ericoides var. microflora. The capacity of L. scoparium to associate with both AM and EcM fungi is well documented (Baylis 1962, Moyersoen and Fitter 1999). Observations of AM in K. ericoides in this study demonstrated for the first time the capacity of dual AM/EcM association in this genus taxonomically close to Leptospermum. The lower AM colonization of K. ericoides var. microflora in prostrate kanuka vegetation in comparison with the greater AM colonization in L. scoparium and K. ericoides var. ericoides in mixed vegetation on cooler soils suggests extreme geothermal conditions are less favorable for growth of AM fungal species present in geothermal areas.
The observation of three Pisolithus species in association with prostrate kanuka and their co-occurrence in the same soil volume (Moyersoen et al 2003) raises this question: How do genetically close EcM fungus species co-occur locally, in association with a single host plant, without mutual competitive exclusion? A possible explanation, already put forward for other organisms (Chapin and Shaver 1985, Tilman 1994), is that these three Pisolithus species differ in investment strategies in reproduction (production of fruit bodies) and vegetative growth (production of EcM and extraradical hyphae). Our observations on EcM morphotypes suggest the three NZ Pisolithus species differ in vegetative growth regarding extramatrical hyphae. Watling et al (1995) already mentioned interspecific variation in the anatomy of rhizomorphs between P. arrhizus and P. aurantioscabrosus. On the other hand, intraspecific differences in rhizomorph development have been observed in Pisolithus EcM (Kammerbauer et al 1989, Lamhamedi and Fortin 1991). The ecological importance of EcM extramatrical mycelium has been demonstrated repeatedly (e.g. Agerer 2001) and interspecific differences in characteristics of Pisolithus rhizomorphs observed in NZ might have important implications in relation with new root colonization and soil foraging capacities.
In addition, the Pisolithus species assemblage in NZ geothermal areas might be influenced by the particular ecological conditions of geothermal areas. For example, soil temperature gradients fluctuate in NZ geothermal areas (Given 1980). These fluctuations might lead to local events of EcM fungi mortality and recruitment. The composition of recruiting species probably is dependent on the available local community or larger metacommunity such as proposed in Hubbell’s neutral theory (2001). Knowledge about the co-occurrence of Pisolithus species in the same area is recent (Hitchcock et al 2003, Moyersoen et al 2003), and no data are available yet on the community structure of Pisolithus in areas where several Pisolithus species co-occur. Knowledge about the community structure and spatial distribution of the three NZ Pisolithus species in geothermal areas is essential to understand how these species co-occur in the same habitat.
In conclusion, Moyersoen et al (2003) proposed that Pisolithus species dispersed several times by transTasman airflow from Australia, where they are distributed over large areas, to New Zealand geothermal areas. The present study showed that the three NZ Pisolithus species form typical EcM associations with prostrate kanuka. The ecological niches acquired by the three Pisolithus species coincide with areas where prostrate kanuka dominates and are characterized by particularly warm, highly acidic and N depleted soil. Understanding how competing species assemble to form a community in the same habitat is a major challenge for ecologists (Tilman 1994, Leathwick 2002). NZ geothermal areas offer an excellent model to understand how ectomycorrhizal species successfully establish in new habitats.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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1 Corresponding author. E-mail: bmoyersoen{at}hotmail.com
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LITERATURE CITED |
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