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Tropical Biology |
2Department of Biological Sciences, University of Rhode Island, Kingston, Rhode Island 02881 USA; 3Department of Agronomy and Soil Sciences, University of Hawaii, Honolulu, Hawaii 96822 USA
Received for publication May 1, 2001. Accepted for publication August 2, 2001.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: arbuscular mycorrhizae • endangered plants • endemic plant species • Glomus aggregatum • Hawaiian soil phosphorus • mycorrhizal dependency • restoration
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Smith and Read, 1996
). However, there has been far less research on the response of native plant species to AMF (Newman and Reddell, 1987
).
The Hawaiian Islands have the highest level of endemism (89%) of any floristic region in the world and include 41% of the endangered plant species listed in the USA (Wagner, Herbst, and Sohmer, 1990
; Mehrhoff, 1996
). One of the major threats to this endemic flora is the loss or destruction of habitats. An important aspect of conservation efforts in Hawaii is the propagation of endemic plant species in greenhouses for later reintroduction to the field. The outplanting of such greenhouse-grown plants to native sites has not been especially successful (Mehrhoff, 1996
). In many of these outplantings, the plants were not mycorrhizal when transferred to the field because AMF were not incorporated into the potting mix in the greenhouse (J. N. Gemma, M. Habte, and R. E. Koske, personal observation).
Because >90% of endemic Hawaiian plant species consistently form arbuscular mycorrhizae (AM) in the field (Gemma, Koske, and Flynn, 1992
; Koske, Gemma, and Flynn, 1992
), it appeared that the lack of AMF at the time of outplanting could be an important component of the failure of plants to become established in the field, especially if plants were transplanted into a soil with a population of AMF below the minimal level (Janos, 1980
). Native Hawaiian soils often are characterized by their low levels of P that is available to plants, a result of the strong P-binding capacity of the volcanic soils (Foote et al., 1972
; Yost and Fox, 1981
). It is in such soils that AMF have been found to be most important to plant growth. However, lack of AMF is not the only explanation for the failures. Other important causes for failure of transplants include seed predation by rodents and other herbivores, competition from alien plant species, and drought (Mehrhoff, 1996
).
While field observations suggest a critical role for AMF in the survival and growth of endemic Hawaiian plants in native soils, there is little experimental evidence to support this view. About 30 plant species were tested in soil-less greenhouse mixes (Koske and Gemma, 1995
), but only two species have been examined in native soils, and both were highly dependent upon AMF in these low-P soils (Miyasaka, Habte, and Matsuyama, 1993
).
The aim of the present study was to examine the response of additional Hawaiian species to inoculation with a native AMF in a native soil. This information could then be used to further assess the hypothesis that the majority of Hawaiian plant species require AMF in low-P soils (Koske, Gemma, and Flynn, 1992
). In addition, because the study included two endangered species, future successful reintroductions of these species would be more likely if their mycorrhizal requirements are known and met when attempts are made to reestablish them in the field.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Fox and Kamprath, 1970
). The soil type is similar to that in which the two Bidens spp. naturally grow, but it was less porous than the soils in which S. tomentosa and C. oppositifolia occur. The soil was air-dried, crushed to pass through a 2-mm sieve and stored in a greenhouse in covered containers for 7 yr. It was not sterilized. Prior to storage, the soil pH was adjusted to 6.75 using dolomite.
In addition to the initial soil-solution P level of the soil (0.005 mg/L), two other target concentrations of soil-solution P (0.020 mg/L and 0.200 mg/L) were established based on a P-sorption isotherm of the soil constructed according to the procedure of Fox and Kamprath (1970)
. The 0.020 mg/L and 0.200 mg/L concentrations were selected because these have previously been found to be the critical levels necessary to classify the mycorrhizal dependency of plant species (Habte and Manjunath, 1991
). Appropriate amounts of KH2PO4 were dissolved in deionized H2O and added to the dried soil just prior to planting to achieve these P levels. The highest P level has been found to result in 95% of maximum yield in many crop species (Fox, 1981
), regardless of the presence or absence of mycorrhizae.
To determine what levels of soil-solution P were common in the Hawaiian Islands, P levels were measured (Fox and Kamprath, 1970
) in 41 root zone soil samples collected in 1998 from various nonagricultural habitats on the islands of Hawaii, Kauai, Maui, and Oahu.
Mycorrhizal inoculation
The mycorrhizal inoculum used in this study was produced using a modification (M. Habte, unpublished data) of the pot culture technique described in Habte and Manjunath (1987)
. In this modified method, a mixture of 90% crushed basaltic sand (Ameron, Honolulu, Hawaii, USA) and 10% calcined montmorillonite (Turface, Applied Industries, Deerfield, Illinois, USA) was used instead of basaltic sand alone in order to supply a slow release of P. Leuceana leucocephala (Lam)DeWit var K636 (Agroforester, Holualoa, Hawaii, USA) was used as the host plant for Glomus aggregatum Schenck and Smith emend Koske (subcultured from a previous pot culture), and the pot culture was grown for 4 mo. A phosphate-free Hoagland's solution (Hoagland and Arnon, 1950
) was applied weekly instead of the nutrient solution used by Habte and Manjunath (1987)
.
This mycorrhizal inoculum, consisting of spores and hyphae of G. aggregatum, infected root pieces of L. leucocephala, and the pot culture medium, was mixed with the soil at the time of planting at a rate of 50 g/kg of soil (dry mass). The control soils were prepared by adding 50 g of sterilized pot culture (basaltic sand plus roots and AMF) to 1 kg soil plus an AMF-free filtrate. The filtrate was obtained by mixing 100 g of inoculum in 1 L of water and passing this suspension through Whatman No. 1 filter paper (Whatman International, Maidstone, UK).
The isolate of G. aggregatum originated from a sample of native Hawaiian soil collected at the Poamoho Experiment Station, Oahu, Hawaii in 1983 (Coltman, Waterer, and Huang, 1988
) and has been maintained in pot culture at the University of Hawaii, Honolulu, Hawaii, USA since then. Voucher specimens have been deposited at the second author's collection at the University of Rhode Island, Kingston, Rhode Island, USA.
Treatments and planting
Seedlings of four endemic Hawaiian species of plants (a coastal shrub, Sesbania tomentosa Hook. & Arnott [Fabaceae]; two wet forest perennial herbs, Bidens sandvicensis (Less) and the naturally occurring hybrid B. asymetrica (H. Lev.) Sherff x sandvicensis [Asteraceae]; and the mesic- to dry-forest tree Colubrina oppositifolia Brongn. ex H. Mann [Rhamnaceae]) were grown in four separate experiments with or without AMF inoculation and at two or three levels of soil-solution P (depending upon the quantity of plant material available). Two of these plant species (S. tomentosa and C. oppostifolia) are federally listed as endangered. The four species were selected for study because they represented a variety of habitats and seeds or seedlings were available. All the species were grown under natural light in a screened greenhouse located at the University of Hawaii Agricultural Experimental Station, Magoon Facility, located in Honolulu, Hawaii, USA (21°18' N and 157°48' W) between September and December, 1998. Water was added as needed to maintain the growth medium at 
60% of maximum water holding capacity.
Plants were grown in tapered plastic forestry tubes ("Conetainers" [Steuwe and Sons, Corvallis, Oregon, USA]) containing 165 mL (133 g) of soil. Five milliliters of a one-quarter strength nutrient solution were added approximately weekly to each "conetainer." The nutrient solution (prior to dilution) was prepared by dissolving the following compounds in 1 L of deionized water: NH4NO3 = 0.143 g; K2SO4 = 0.2965 g; MgSO4 middot; 7H2O = 1.09 g; ZnSO4 · 7H2O = 0.044 g; CuSO4 · 5H2O = 0.0195 g. Separate solutions were made of Na2MoO4 · 2H2O (0.00125 g/L) and Na2B4O7 · 10H2O (0.007 g/L) (M. Habte, unpublished data). The one-quarter strength was used because of the known sensitivity of endemic Hawaiian plants to full strength fertilizer solutions (Wooliams, 1976
; Koske and Gemma, 1995
).
Two experiments (with S. tomentosa and B. sandwicencis) followed a randomized complete block design with a 2 x 3 factorial combination of treatments (two levels of mycorrhizal inoculation [with or without inoculation] and three soil P levels [0.005, 0.020, and 0.200 mg/L]). Seeds of S. tomentosa were scarified by nicking the seed with a razor and soaking the seeds overnight in tap water prior to placing them on sterile, wet filter paper (Whatman #1) in glass petri dishes (150 x 20 mm) until germination (4 d). One seedling was placed in each "conetainer," with eight replicates per treatment. This experiment lasted 72 d.
Seeds of B. sandwicencis were sown on water agar (1.5%) until germination (10–14 d) when they were transferred to shallow aluminum trays containing Sunshine Mix No. 1 (Fison's Horticultural, Vancouver, British Columbia, Canada) for 8 d. One seedling was then placed in each "conetainer," with six replicates per treatment. Plants were grown for 58 d.
The experiment with C. oppositifolia followed a 2 x 2 randomized complete block design (two levels of mycorrhizal inoculation [control and inoculated] and two soil P levels [0.005 and 0.200 mg/L]) with six replicates per treatment. Seeds of C. oppositifolia were nicked with a razor blade, soaked overnight in warm tap water, and planted in shallow plastic trays filled with Sunshine Mix No. 4 and coarse pumice stone. The seedlings were grown for several weeks on screen-covered benches in natural light at the Lyon Arboretum (Manoa, Hawaii, USA) in August 1998 (A. Yoshinaga, University of Hawaii, personal communication), before being transplanted to the "conetainers" at the start of the experiment. Plants were grown in "conetainers" for 88 d.
The design for B. asymmetrica x sandvicensis was a randomized 2 x 2 complete block design with six replicates per treatment. The treatments consisted of two levels of mycorrhizal inoculation (control and inoculated) with or without a seaweed-based organic amendment (GroWin, Ocean Organics, Waldoboro, Maine, USA). The GroWin (7 : 3 : 1 [NPK]) was applied at 2.5 g/L of soil, mixed throughout the contents of the "conetainers." GroWin was included in this study because it had been shown to significantly enhance the effect of AM on the growth of turfgrasses (J. N. Gemma and R. E. Koske, unpublished observation). After adding the GroWin to the soil, soil-solution P was measured (Fox and Kamprath, 1970
) in the amended and unamended media. The soil-solution P was the same in both, 0.005 mg/L. Nutrients were applied as described above, and the seeds and seedlings of B. asymmetrica x sandvicensis were germinated and transplanted in the same manner as for B. sandvicensis. Plants were grown for 75 d.
Measurements taken
The effects of inoculation and soil-solution P were assessed by several parameters. Shoot dry matter was determined after drying plant samples for 24 h at 70°C. Root dry matter was determined after roots were air-dried at room temperature (22°C) in an air conditioned room until a constant mass was obtained (2–3 d). Roots were not oven-dried because they became too brittle for staining and assessment of colonization. Plant heights (soil surface to the terminal bud) were recorded throughout the course of the experiment for all species except the semi-prostrate S. tomentosa. The P concentration of leaf pinnules (S. tomentosa) or of 6.3-mm diameter leaf disks removed from the youngest fully expanded leaf was measured at the end of each experiment (Habte, Fox, and Huang, 1987
). Flowering was not evaluated because plants did not flower during the experiment. Mycorrhizal colonization of air-dried roots was determined using the grid-line intersect method (Giovannetti and Mosse, 1980
) after clearing in 2.5% KOH and staining with trypan blue (Koske and Gemma, 1989
).
Statistics
Data were log-transformed using the formula [ln (x + 1)] if homogeneity of variances could not be assumed (Bartlett's homogeneity of variance test). Data were then analyzed using one- or two-way ANOVA, as appropriate (AndersonBell, 1983
). Statistical significance was assigned at P < 0.05.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Leaf tissue P increased significantly in response to inoculation (P < 0.001) and to soil P concentration (P < 0.001) (Fig. 2). The benefit of inoculation was greatest at the lowest P concentration (three times larger) but was lost at the higher concentration of soil P. Interaction between P and inoculation on leaf P was significant (P < 0.001).
Root colonization by AMF appeared to be unaffected by soil phosphorus levels as colonization was >90% for inoculated plants in all three phosphorus treatments. No colonization was present in the noninoculated plants.
Bidens sandvicencis (three levels of soil P and inoculation)
Shoot dry matter production of B. sandvicensis was significantly increased in response to inoculation (P < 0.01) and increasing levels of soil P (P < 0.001). Root dry mass was enhanced significantly by P level (P < 0.001) but not by inoculation. At the two lower P levels, inoculation greatly enhanced growth (Figs. 2–4), and inoculated plants were up to 3.3 times (shoots) and 16.7 times (roots) larger than controls. Noninoculated plants did not increase root growth appreciably in response to increasing soil P until concentrations were above the level of 0.020 mg/L (Fig. 4). Leaf tissue P significantly increased in response to inoculation (P < 0.001) but not in response to increasing soil P levels (Fig. 2).
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Shoot height increased significantly in response to inoculation (P < 0.001) and increasing soil P levels (P < 0.001). Inoculated plants at 0.020 mg P/L were 3.2 times taller than controls (Fig. 5A). The interaction between inoculation and soil-solution P also was significant (P < 0.003).
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Colubrina oppositifolia (two levels of soil P and inoculation)
Dry matter production of both shoots and roots of C. oppositifolia increased significantly in response to inoculation (P < 0.01 and P < 0.001, respectively) and to added soil phosphorus (P < 0.05 for both) (Figs. 2 and 6). Leaf tissue P was not significantly affected by inoculation or P level in the soil (Fig. 2).
No significant interactions between inoculation and soil P level were observed. Shoot height increased significantly (1.3 to 1.6 times) in response to inoculation (P < 0.002) and increasing soil P levels (P < 0.01) (Fig. 5B). Interaction between inoculation and soil-solution P was not significant. Root colonization was >90% in all inoculated treatments. No colonization was present in the noninoculated plants.
Bidens asymetrica x sandvicensis (organic amendment and inoculation)
Shoot height and shoot and root dry mass of B. asymetrica x sandvicensis were enhanced significantly in response to inoculation (P < 0.001 for all three) and to the addition of GroWin (organic amendment) (P < 0.011, P < 0.001, and P < 0.001, respectively) to the native soil (0.005 mg P/L) (Figs. 5C and 7). Yield increased over control plants 5 times when either inoculum or organic amendment was included in the treatment and 26 times if both AMF and GroWin were added to the native soil, which is indicative of significant interaction (P < 0.015 for height, P < 0.01 for shoot mass, and P < 0.05 for root mass). There was significantly more foliar P in the inoculated treatments (P < 0.05) (Fig. 8), but the addition of GroWin had no significant effect on foliar P.
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P levels in native soils
The soil-solution P levels of the 41 native soils were very low, ranging from undetectable (<0.001 mg/L) to 0.030 mg/L, averaging 0.010 
± 0.007 (1 SD) (Table 1).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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).
Using the criteria of Habte and Manjunath (1991)
for categorizing mycorrhizal dependency (MD), S. tomentosa would be rated as "highly dependent" and B. sandvicensis as "very highly dependent." The other two species were not tested over the range of soil-solution P levels needed to assign a dependency level.
Results from the present study suggested some modification in the terminology for describing the MD of nonagricultural species. The calculated MD of a species depends in part upon the soil-solution P to which the plant is exposed (e.g., Plenchette and Morel, 1996
), and MD values measured in native soils do not match those from agricultural (high-P) soils. For the Hawaiian species, the MD at soil-solution P levels of 0.005–0.020 mg P/L is a far more important parameter for use in habitat restoration than the MD at 0.200 mg P/L. Response of native plants (endemic and indigenous species) to AMF at 0.200 mg P/L provides information that has horticultural value, but is not relevant to plantings in field soils (i.e., nonagricultural). To focus on the necessity of assessing MD at appropriate soil-solution P levels, we suggest the term "ecological mycorrhizal dependency" (EMD), a value based on growth in soils with soil-solution P levels similar to those encountered by plants in the field. For species grown under agricultural conditions, the term "agricultural mycorrhizal dependency" (AMD) is appropriate. This value would be calculated from results in soil containing 0.200 mg P/L in soil solution and would be most suitably applied to crop species.
The EMD values (for soil-solution values of 0.005 and 0.020 mg P/L) for the four species in present experiment ranged from 44 to 88%, indicating high dependence on AMF when grown in native soils. Two other endemic Hawaiian species (Acacia koa and Sophora chrysophylla) had EMD values of 37 and 71%, respectively (Miyasaka, Habte, and Matsuyama, 1993
).
As reported in many earlier studies (see Smith and Read, 1996
), high levels of soil P often negate any growth enhancement by AMF. Such an effect was noted in three of the four species the present study. When the concentration of soil-solution P was at the level of highly productive agricultural soils, the benefits of inoculation were minimal with the exception of C. oppositifolia. As the analysis of soil-solution P levels from a variety of nonagricultural sites showed, however, it is unlikely that native Hawaiian species will encounter sufficiently high P levels in native habitats to render AMF nonessential. A soil sample collected from the field beneath S. tomentosa had a soil-solution P level of 0.011 mg P/L, and a sample from the root zone of B. sandvicensis had 0.027 mg P/L (Table 1).
A previous report of the routine occurrence of AMF in roots of 46 endemic Hawaiian species (including S. tomentosa, and B. sandvicensis) led to the suggestion that most endemic species in Hawaii are highly dependent upon AMF in their natural habitats (Koske, Gemma, and Flynn, 1992
). Findings from the present growth study and that of Miyasaka, Habte, and Matsuyama (1993)
support this view. A previous study of the effects of the AMF G. intraradices on growth and survival of Hawaiian plant species indicated that 20 of the 30 native species tested responded significantly to inoculation (Koske and Gemma, 1995
). The latter trials employed several types of growth media, and soil-solution P levels were not always comparable to the levels in the field, preventing a direct comparison with the present study.
Four other species of Sesbania (not native to Hawaii) have been investigated for their MD in Hawaiian soils with the same isolate of G. aggregatum used in the present study and were found to range from moderately to marginally dependent (Habte and Aziz, 1985
; Habte and Manjunath, 1991
), in contrast to the high dependency of the endemic species, S. tomentosa. In that study, the EMD of the non-Hawaiian species grown for 40–65 d at 0.020 mg P/L ranged from 15 to 35% (mean 26%). In comparison, EMD of S. tomentosa was 50% at the same soil-solution P level.
The inability of high levels of P to replace AMF in C. oppositifolia was noted in an earlier study of this species. In that study, plants that had been grown in a peat-based greenhouse mix (AMF-free) for 210 d were separated into two groups, one inoculated with the AMF G. intraradices, the other left as a control. Eight months later the controls were dead and the inoculated plants were thriving (Koske and Gemma, 1995
).
While high levels of phosphate in the soil can decrease root colonization (e.g., Bolan, Robson, and Barrow, 1984
; Habte and Manjunath, 1991
; Miyasaka, Habte, and Matsuyama, 1993
), root colonization was not affected significantly by P level in this study. The relative uniformity of colonization in the present study across the P range tested may result from the plants having grown for 2–3 mo in small containers that ensure more frequent contact between an active hyphal network and new roots.
The enhanced rooting resulting from inoculation at soil-solution P levels equivalent to those of native soils was especially remarkable (Fig. 4). Large root systems provide improved access to soil nutrients as well as to water. Although the Hawaiian Islands are tropical, drought is not uncommon (e.g., Egler, 1947
; Richmond and Mueller-Dombois, 1972
), and enhanced tolerance to drought would have significant effects on survival. Numerous studies document instances of AMF providing increased drought tolerance in a variety of species (e.g., Nelsen, 1987
; Smith and Read, 1996
; Gemma et al., 1997
).
Enhanced rooting may increase the survival rate of transplants, and pretransplant inoculation with AMF has been shown to improve growth and reduce transplant injury, especially when transplants were grown in a low-P soil or were exposed to high temperatures or arid conditions (e.g., Barrows and Roncadori, 1977
; Menge et al., 1978
; Biermann and Linderman, 1983
; Vosatka, 1995
). While greenhouse studies of Hawaiian plants with AMF have suggested a vital role for AM in establishment of plants, there is a need for field trials to confirm greenhouse observations. In a study undertaken recently (see Miyasaka and Habte, 2001
), the establishment and growth of A. koa on a former pastureland in Hawaii, USA, was significantly improved by inoculation of seedlings with AMF in the nursery.
The striking enhancement of the growth of B. asymmetrica x sandvicensis in response to the combination of AMF inoculation and the organic amendment GroWin was unexpected. The mechanism for this synergistic effect is unknown but may be a result of the variety of additional nutrients provided by the GroWin. The same effect has been found in inoculated turfgrass species grown in a sand : sphagnum peat mix (4 : 1 vol : vol), a substrate with no P-binding capacity (J. N. Gemma and R. E. Koske, unpublished observation). In the turfgrass studies, the effect of GroWin could not be replaced by additions of P or N. GroWin may be useful in future restoration efforts, both in the greenhouse and during outplanting into field soils.
The results of the present study and other studies on the mycorrhizal status and growth responses of Hawaiian plants to inoculation with AMF (Koske, Gemma, and Flynn, 1992
; Miyasaka, Habte, and Matsyama, 1993
; Koske and Gemma, 1995
; Miyasaka and Habte, 2001
) support the hypotheses that endemic Hawaiian species evolved in P-limited soils and that the majority of the nearly 1000 extant species are derived from founder species with high EMDs (Koske, Gemma, and Flynn, 1992
). As a consequence, it appears essential when restoring or augmenting plant communities to ensure that endemic species are inoculated before or during outplanting to native soils that are lacking AMF or have low mycorrhizal inoculum potential (Miyasaka and Habte, 2001
). Such soils are likely to be found in disturbed or barren sites (e.g., Jasper, Abbott, and Robson, 1989
), the very sites likely to require restoration.
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FOOTNOTES |
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4 Author for reprint requests (jgemma{at}uriacc.uri.edu
).
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