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Ecology |
Department of Biology, Swarthmore College, Swarthmore, Pennsylvania 19081 USA
Received for publication October 15, 2002. Accepted for publication February 20, 2003.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: Beta vulgaris • Chenopodiaceae • Convolvulaceae • Cuscuta salina • parasite • predisposition • salinity • specialization • stress • susceptibility • zonation
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Dawson et al., 1990
), which of course is strongly influenced by environmental conditions. In many instances, it could be argued that large, rapidly growing hosts existing under optimal conditions would represent a good source of material for attached parasites, partially because the host size represents a large potential resource. On the other hand, parasite growth might be especially rapid on stressed hosts if the stress in question resulted in decreased allocation to morphological and chemical defenses (reviewed in Gershenzon, 1994
). Furthermore, stressed plants may be surprisingly good hosts, despite being small, because they possess more concentrated stockpiles of metabolites that are not being allocated to growth (Nunes et al., 1984
; Wyn Jones, 1984
; Rabe, 1990
; Araya et al., 1991
; Munns, 1993
) and because they accumulate additional carbon- and nitrogen-containing compounds such as polyols, proline, and glycinebetaine that act as osmoprotectants, compounds that protect various aspects of cell physiology from the consequences of osmotic stress (Ackerson, 1981
; Neales and Sharkey, 1981
). Although host breadth and host specialization are traditionally viewed with respect to host species taxonomy, it is possible that certain parasitic plants may specialize on plants that are suffering from a particular type of environmental stress.
Cuscuta salina (saltmarsh dodder, Convolvulaceae) is a leafless holoparasite found primarily in salt marshes of coastal western North America, inland salt flats, and occasionally alkaline meadows (Flowers, 1934
; Yuncker, 1965
; Vogl, 1966
; Beliz, 1986
) and is an ideal species for studies on environmentally mediated host predisposition to parasitic attack. Traditional explanations of the patterns of distribution and zonation of C. salina have cited the co-occurrence of halophytic Chenopodiaceae species (especially Salicornia spp.) and C. salina as strongly suggestive of host preference for members of this highly salt-tolerant family. Beliz (1986)
believes that this association may be easily explained by the low diversity of vegetation in saltmarshes (i.e., by default, C. salina must grow on Chenopods) rather than by specialization on Salicornia and related species. In support of this view, dense stands of Salicornia individuals, the purported "preferred host" of C. salina, are sometimes entirely free of dodder infection (Vogl, 1966
), implicating instead a direct or indirect effect of environmental constraints on dodder distribution (Cummins and Deutschman, 2000
; St. Omer, 2001
). Although salinity variation across saltmarsh areas is mentioned in many descriptions of C. salina distribution, salts and other soil factors are unlikely to act directly on dodders except during seed germination and during a brief seedling stage, after which soil contact is lost and attached dodder seedlings become completely dependent on their host for nutrients as well as water. Salt and other dissolved ions may, however, act indirectly on the growth rate of this dodder by altering the initial susceptibility and subsequent suitability of hosts to parasitic attack, via one or more of the mechanisms described earlier. If saltmarsh dodder is indeed a "stress specialist," it may be possible to better explain why dodder is excluded from certain parts of the salt marsh even though suitable and preferred host species (e.g., Salicornia spp.) may be found growing there (Pennings and Callaway, 1996
).
Alternatively, habitat restriction of C. salina may be related to factors unassociated with host preference and host suitability. Mature fruit of Cuscuta species typically remain tightly adhered to the host stem and would likely remain attached to broken parts of hosts that are deposited in wrack, the redeposited plant material that is important in saltmarsh plant recruitment (Ellison, 1987
). Dodder fruit also tend to float (C. B. Purrington, personal observation). These avenues of water-dependent dispersal (hydrochory), as well as marsh-to-marsh dispersal by birds (ornithochory), may be very important in saltmarsh dodder distribution and zonation, as has been hypothesized for riparian-associated dodder species (Burkart, 2001
). Furthermore, C. salina could possess salt-dependent germination cues that might reduce establishment in areas with low or extremely high salinity.
We evaluated the following questions: (1) Is reproductive fitness of dodder greatest when grown on hosts subjected to salinity stress? (2) Are host solutes (sugars, ions, nitrates) more concentrated at a particular salinity? (3) Is germination of saltmarsh dodder dependent upon salt concentration? We hypothesized that fitness of dodder would increase with increasing concentrations of sodium chloride because hosts would possess elevated metabolite concentrations in their leaves and stems compared with hosts grown with no salinity. We further hypothesized that the effects of salt on C. salina germination would be inhibitory, as noted for other halophyte seeds (Ungar, 1978
), and thus would not explain the rarity of this species in nonsaline areas.
These investigations involve the use of beet (Beta vulgaris) as a host because it is an easily grown chenopod and because it is heavily damaged by dodder infestations, especially in the countries of the former USSR and arid regions of the United States (Ashton and Santana, 1976
). Although some of the physiological and morphological characteristics are probably the result of artificial selection, beet is sexually compatible (Bartsch and Ellstrand, 1999
) with the sea beet (Beta vulgaris subsp. maritima = Batis maritima), which grows in the salt marsh zone frequented by C. salina (Vogl, 1966
) and is tolerant of hypersaline soils (Pennings and Richards, 1998
). The use of B. vulgaris is thus likely to yield ecologically relevant information about the interaction of saltmarsh dodder with halophytic members of the Chenopodiaceae, the family most often suggested as the preferred host of C. salina.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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to induce salt stress in Beta vulgaris. Although higher salinities (e.g., at seawater levels, at 32 ppt; and elevated marsh areas where evaporation concentrates dissolved ions) would have been appropriate for hosts native to salt marshes, for domesticated beet, 14.6 ppt is likely to induce a very high salt stress. Actual salinity in each pot was not monitored, but the buildup of salt beyond the target concentrations was minimized by watering each pot once per week with large volumes of fresh water prior to application of the appropriate salinity solution. Greenhouse temperature during the experiment was approximately 21°C and day length was 14 h, with additional lighting provided by sodium vapor lamps. One-half of the beets (44 plants total, with 11 plants at each salinity level) were randomly assigned to the parasitization treatment, with tendrils of C. salina collected from a single clone (derived from seed collected in 1993 at Bodega Bay, California, USA) growing on Chenopodium album. Parasites that died before successfully attaching to their hosts were replaced with a new tendril until 11 beets at each salinity regime were supporting dodder (for image of infected beet, see the Supplemental Data accompanying the online version of this paper). After 14 wk, when the leaves of the hosts had senesced, all flower buds and fruits produced by C. salina were counted, and the roots of all beets were cleaned, dried, and weighed to the nearest 0.0001 g.
The effect of salinity on root mass of Beta vulgaris was analyzed with one-way analysis of variance (ANOVA) followed by multiple comparisons (Fisher's protected LSD tests) to examine differences among means. Because of the nonnormality of parasite fecundity data, the effects of host salinity on dodder were analyzed with a Kruskal-Wallis test, followed by nonparametric multiple comparisons (Mann-Whitney U tests).
Effects of salinity on host stem content
During the summer of 2002, 160 seedlings each of carrots (Daucus carota; Apiaceae) and beets (Beta vulgaris; Chenopodiaceae) grown in 10 x 10 cm square plastic pots were randomly assigned to four salinity treatments in the Swarthmore College greenhouse: 0, 100, 250, and 400 mmol/L NaCl (a greater range of salinity was used in this experiment because the 250 mmol/L level in the above experiment, conducted earlier, was still reasonably tolerated by beets). After approximately 28 d, stem fluid was obtained from each plant with a hydraulic plant press (Spectrum Technologies, Plainfield, Illinois, USA) and then analyzed for total soluble sugars (Atago PR-32 refractometer, Japan), total nitrates (Cardy Nitrate Meter, Horiba Inc., Kyoto, Japan), and conductivity (Horiba Twin Cond meter, Horiba Inc.). Dry mass of all roots was also determined (as an estimate of the degree of salt stress in each treatment). All measurements were analyzed with ANOVA, with Fisher's protected LSD multiple comparisons applied when main effects were significant.
Effects of salinity on dodder germination
Ten seeds of C. salina were placed in 15 x 60 mm petri dishes filled with 10 mL of a salt solution (either 0, 62.5, 125, or 250 mmol/L NaCl). Ten replicates of each salinity level were situated in random positions within a growth chamber maintained at 21°C with 18-h days. Solutions were drained and replaced every 2 d to minimize changes in salinity from evaporation. Germination was censused daily for 16 d. Ungerminated seeds were not assessed for viability.
The number of seeds germinating at different salinity levels was analyzed with a one-way ANOVA on arcsine square-root transformed percentages of replicate petri dishes. Mean time to germination was computed for each petri dish and analyzed with ANOVA.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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level adjusted for six multiple comparisons, P < 0.0085). The difference in dry mass of beet roots at the two intermediate salinities was marginally significant given this adjusted level (Fisher's protected LSD, P = 0.0193).
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Effects of salinity on host stem content
The effects of salinity, set up to include a wider range of salt concentrations (0–400 mmol/L) than the above experiment, showed effects on all three stem components measured, with similar responses observed in both B. vulgaris and D. carota (Table 1, Fig. 2). Sugar concentrations in stem tissue of plants grown at all salinity levels were significantly elevated compared to the mean concentration in plants watered with fresh water (Fisher's protected LSDs with adjusted to 0.0082 for six comparisons). Nitrate content did not show this pattern, however, but was higher in stems of plants at the 250 mmol/L NaCl treatment (Fisher's protected LSD, P = 0.0027). Conductivity, a rough measure of the concentration of all ions in a solution, increased linearly in response to increasing salinity, although the adjustment for multiple comparisons reduced the significant difference to tests of 0 vs. 250 mmol/L NaCl plants and of 0 vs. 400 mmol/L NaCl plants (Fisher's protected LSDs, P = 0.0072 and P = 0.0002, respectively; all other P > 0.0085).
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adjusted to 0.017; all P = 0.001).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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), and thus emergence of C. salina in even more saline zones, such as areas in which evaporation has greatly concentrated the deposited seawater, would be further reduced. We hypothesized that C. salina growing on salt-stressed hosts would show more vigorous clonal growth and attain higher levels of reproductive output. Our results provide partial support for this view. We found that C. salina fitness on Beta vulgaris receiving regular treatment with the highest salinity (250 mmol/L NaCl) was more than double the reproductive fitness of C. salina on hosts grown at the two lower salinity regimens (62.5 and 150 mmol/L NaCl). If halophytic species in salt marshes behave similarly as hosts for C. salina, parasites growing in particular zones of the salt marsh may produce proportionately more seeds. Because dodder fruit remain attached to host plants, subsequent dispersal into other zones of higher and lower salinity may be minimal, further reinforcing a zonation pattern.
Our data on stem contents support the view that salt-stressed B. vulgaris (and D. carota), although generally smaller, contain high concentrations of solutes (e.g., carbohydrates and nitrogen-containing compounds) that are likely to be important for dodder growth and reproduction (Fer, 1981
). Total dissolved sugars, nitrates, and ions were elevated in the 250 mmol/L NaCl treatment, the salinity that resulted in high dodder reproductive output. At the highest salinity in the stem content experiment (400 mmol/L NaCl), stem concentrations of sugars and total ions remained unchanged, and nitrate levels fell, together suggesting that salinity increases beyond 250 mmol/L NaCl may not increase the nutritional status of B. vulgaris plants for attached C. salina. Therefore, although our experiment examining dodder success was restricted to salinities between 0 and 250 mmol/L NaCl, we would predict that further experimentation at salt levels beyond 250 mmol/L NaCl would reveal a decrease in dodder reproductive output. Similarly, our finding of a potential peak for stem contents in response to salinity variation could explain why C. salina is rarely found in areas of the salt marsh with extremely high salinities, even though potential host plants exist there.
Despite the support for our general prediction, that salt stress will lead to increased dodder performance, we found that the reproductive success of C. salina growing on salinity-free B. vulgaris was also high, indeed indistinguishable from the reproductive output of parasites grown on the most salt-stressed hosts. The dry mass of these salinity-free hosts (or their parasite-free equivalents, rather) was indistinguishable from B. vulgaris plants grown at the lowest salinity, 62.5 mmol/L NaCl, suggesting that the increased success of dodder on the control (salt-free) hosts is not easily attributed to the large size of the hosts grown at 0 mmol/L NaCl. As a possible explanation of the high dodder fecundity when cultured on control (0 mmol/L NaCl) plants, it is conceivable that saline water may have occasionally splashed directly onto dodder tendrils in all the salt-containing treatments and thus directly reduced dodder growth. We have not assessed the effects of salt spray on dodder growth, but identify such measurements as valuable in further studies on the zonation pattern of C. salina.
Because we have shown that C. salina is able to thrive on halophytic hosts grown free of salinity stress, its restriction to salt marshes may be explained by mechanisms other than physiological unsuitability of potential hosts. One possibility is that C. salina, like other dodders, remains firmly attached to host stems even after the host senesces. Therefore, when host stems are broken by wave action, they can be redeposited along with any attached C. salina fruit when high tides leave wrack at higher elevations of a salt marsh (Hopkins and Parker, 1984
; Ellison, 1987
; Pennings and Richards, 1998
). However, explanations such as this cannot explain why rare dispersal events of C. salina seeds to nonsaline areas, events which must surely take place, have not resulted in at least some persistent extra-marsh populations. That there are no published reports, to our knowledge, of C. salina growing in nonsaline areas suggests that some other aspect of the natural history (e.g., early seedling growth and attachment or adult clonal growth, neither of which we studied) is contingent upon the presence of salinity. Other ecological factors, such as different host distributions and competition from other phloem parasites (e.g., aphids) could further reduce the success of C. salina seeds that are deposited outside of saline areas. For the rare, successful escape from the salt marsh, it is possible and perhaps likely that populations would go unnoticed or be misidentified. This latter scenario is always a concern in research on Cuscuta spp. from the reliance of taxonomic keys on rather minute differences in flower and fruit morphology and from the importance of collection habitat (Beliz, 1986
).
Callaway and Pennings (1998
; reviewed in Pennings and Callaway, 2002
) have shown that C. salina tendrils have a reduced tendency to coil around Anthrocneum subterminale when also presented with Salicornia virginica in a "choice test." Because A. subterminale typically occurs in a less saline zone adjacent to a lower-elevation, higher-salinity, Salicornia-dominated zone, their results suggest that nonrandom foraging behavior of tendrils may limit the advance of C. salina into less saline areas of the salt marsh, foraging that could be based on the reported ability of Cuscuta spp. to perceive differences in nitrogen levels and quality between available hosts (Kelly, 1990
, 1992
). Future research, however, must be conducted to determine whether this nonrandom host selection is in part imprinted by the source (here, S. virginica) of the tested tendrils (Callaway and Pennings, 1998
), rather than from host selection based on species differences or variation in the salinity of host environment. Given their general result, however, it would be desirable to conduct further experiments on host choice and host suitability using a wider variety of host species, especially those that occur in the A. subterminale zone, which is reported to be free of salt marsh dodder (Callaway and Pennings, 1998
), and in those zones that are only slightly saline or nonsaline but still close to the salt marsh. In particular, it is unknown whether nonhalophytic species, the dominant vegetation in nonsaline areas, would also support high parasite growth. We have successfully cultured C. salina on nonhalophytic host plants (e.g., Impatiens spp., Coleus spp.) under greenhouse conditions, so there does not seem to be any strong incompatibility present against host species that are not salt tolerant.
In summary, we found that germination of C. salina was not dependent on salinity, and thus zonation patterns of this parasite cannot be directly attributed to the effect of variation in salt concentration on seed emergence. We have also shown that salt-stunted host plants can function as surprisingly good hosts given their small size, a finding that matches field observations and reports of luxuriant growth in moderately saline areas of salt marshes (Sanderson, 1998
; Sanderson et al., 2000
). Our data on stem contents, collected on both D. carota (carrot) and B. vulgaris (beet), suggest that stunted plants are rich in nutrients that are important for dodder growth.
More generally, investigation of environmentally mediated host susceptibility may explain distribution patterns of other members of this genus that appear to be restricted to certain dry or saline areas (e.g., C. nevadiensis, C. sandwichiana, C. vivipara) or to flooded or moist areas (e.g., C. gronovii). Because drought and flooding stress often result in the accumulation of sugars and nitrogen-containing osmoticants (Wallace et al., 1980
), certain members of Cuscuta may specialize on hosts suffering moderate amounts of stress. Cuscuta indecora, which has been reported in brackish areas of eastern United States (Musselman, 1986
; Silberhorn, 1998
), might be similar to C. salina in its ability to grow on salt-stressed hosts. Other species are hypothesized to have a preference for host species such as legumes and mints that have a high baseline amount of nitrogenous compounds (Salageanu and Fabian-Galan, 1968
), and Kelly (1992)
has shown that some dodders have the ability to reject hosts with low nitrogen content. Therefore, although there is growing consensus that Cuscuta species are not parasitic generalists (Kuijt, 1969
; Kelly et al., 1988
), our results suggest that part of the perceived specialization in some members of the genus is instead dictated by underlying environmental conditions that affect susceptibility of specific host species.
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FOOTNOTES |
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2 Present address: Laboratorio de Estudios Ambientales. Instituto de Zoología Tropical. Facultad de Ciencias. Universidad Central de Venezuela. Apartado 47058. Caracas, 1041-A. Venezuela
3 Author for reprint requests (Tel.: 610 328-8621; Fax: 610 328-8663; purrington{at}swarthmore.edu
)
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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