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Departamento de Ecología Evolutiva, Instituto de Ecología, UNAM, A.P. 70-275, Mexico 04510, D.F., Mexico
Received for publication September 3, 1999. Accepted for publication June 22, 2000.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: herbivory • infection • leaf-pathogens • Los Tuxtlas • tropical rain forest • understory
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). In contrast, information on plant–pathogen interactions in natural systems, particularly in tropical rain forests, is very scarce and only a handful of studies is available (see Coley and Barone, 1996
; Gilbert and Hubbell, 1996
; Lodge, Hawksworth, and Ritchie, 1996
). Available data suggest that the incidence of diseases is higher in tropical crops than in temperate ones, and it is argued that this is partly due to the more suitable conditions of tropical zones for pathogens (Waller, 1976
; Shivas and Hyde, 1997
). No available evidence exists to assess whether such tropical–temperate differences in agronomic systems are applicable to natural ecosystems (see Coley and Barone, 1996
).
The mesic and shady environment, together with the density of foliage coverage found in the understory of tropical rain forests (cf. Dirzo et al., 1992
), are expected to be particularly appropriate for the development of plant pathogens (see Augspurger, 1983, 1984
), including leaf pathogens. Some preliminary observations in the rain forest of Los Tuxtlas, Veracruz, Mexico (Dirzo, 1987
; de la Cruz and Dirzo, 1987
) support this expectation. However, to our knowledge, no quantitative assessments exist of the incidence of leaf pathogen infection at the plant community level in tropical rain forests. In these communities, incidence of leaf pathogen infection would be expected to vary with time, according to the seasonal variation in rainfall (Soto and Gama, 1997
), and with space (García-Guzmán et al., 1996
), according to ecological heterogeneity such as that imposed by light availability or microsite floristic composition (e.g., low vs. high local density and species diversity; Dirzo et al., 1992
). Overall, it could be expected that the wettest period and the more shaded microsites of the forest should lead to greater pathogen infection (Burdon, 1987
).
Another major gap in knowledge about plant–pathogen interactions in natural tropical systems concerns the proximal mechanisms of leaf infection. Studies in agricultural systems and in some temperate forests have shown that leaf damage by pathogens with life-histories such as that of the nonsystemic airborne fungal pathogens appears to be associated in many cases to damage by herbivores, mainly insects (Manners, 1993
). Given the enormous diversity and abundance of phytophagous insects (Erwin, 1982
) and the prevalence of herbivory in tropical rain forests (Howe and Westley, 1988
; Coley and Barone, 1996
), it is possible that such animals may play a significant role in the incidence of disease in the plants of these forests. It is known that insects can promote pathogenic infection either by active transportation and inoculation of spores (Manners, 1993
) or by causing physical damage that then facilitates penetration of pathogenic inoculum (Dirzo, 1987
; García-Guzmán, 1990
).
In the present study we address two issues basic to the study of plant–pathogen interactions in tropical forests. The first issue concerns documentation of the incidence of leaf damage by pathogens based on a quantitative survey of the extent of leaf damage in understory plants of the Los Tuxtlas tropical rain forest. Such analysis focuses specifically on the following questions: what is the overall magnitude of damage by pathogens and its variation among species and is there variation in the incidence of pathogen damage in relation to the seasonal and spatial variation of this forest? The second issue addresses the association of damage by pathogens and herbivores, with the aim of exploring the following question: does insect herbivory play a role on the incidence of pathogenic disease symptoms in the forest understory?
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). The region is hot and humid; mean monthly temperature is 27°C, but it ranges from 17°C (January) to 29°C (June). Annual rainfall averages 4750 mm with a relatively dry season (April–May) during which rainfall drops to 
200 mm and a very wet season from June to February (Soto and Gama, 1997
). The vegetation of the area is classified as "high evergreen rainforest" (Pennington and Sarukhán, 1998
), characterized by evergreen vegetation and trees exceeding 30 m. The forest understory is composed of seedlings and saplings of trees, palms, shrubs, lianas, and herbaceous plants, as well as the young stages of climbing vines. The most abundantly represented plant families include Araceae, Bignononiaceae, Euphorbiaceae, Leguminosae, Moraceae, Orchidaceae, and Piperaceae (Ibarra et al., 1997
). Detailed accounts of the natural history of the area are given in González, Dirzo, and Vogt (1997)
.
Incidence of leaf damage
To assess the levels of damage by leaf pathogens and their occurrence in terms of the species that characterize the understory community and the season of the year, we selected four sites of mature forest (without treefall gaps) on relatively flat areas. Bearing in mind these criteria of forest age and topography, the four sites were chosen on the basis of the local dominance of a particular plant species along each of the four major trails of the field station (see García-Guzmán, 1990
). Such local dominance was defined by the clumped distribution and high local density of a given species of tree and a predominance of seedlings and saplings of the same tree (see Dirzo and Miranda, 1991
). The local dominant tree species in each of the sites were Dussia mexicana (site 1), Nectandra ambigens (site 2), and Omphalea oleifera together with Brosimum alicastrum (sites 3 and 4). In addition, the four sites differed in the degree of shading in the direction of site 2 (most shaded) > site 1 > site 3 > site 4 (least shaded). Degree of shading was estimated by Dirzo et al. (1992, and R. Dirzo, unpublished data) with black-and-white hemispherical (fish-eye)-lens canopy photographs, using a Sigma Fisheye Lens (1:4, F = 8 mm). In each site a sampling plot was established by means of a 50 m north–south straight line. Along the line, ten randomly selected points were chosen. On each of these points we established 5-m long transects, perpendicular to the central line. Their position (right or left of the 50-m line) and distance from the origin were selected at random. The survey was carried out using a variation of the point–quadrat technique for sampling species composition and coverage (Greig-Smith, 1983
). Along the 5-m transects we located 25 points by the random positioning of a descending needle; all plants <1 m height touched by the tip of the needle were recorded and all their leaves collected for subsequent analysis of pathogen damage and herbivory in the laboratory (see below). There were 250 sampling points per site. Each sampling point included all plants touched by the descending needle or no plants if the needle did not touch any plant. The survey was carried out during the latter part of the rainy (November) and the peak of the dry (April) seasons, with sampling plots independently established in each of the two seasons.
With this sampling protocol we were able to obtain average levels of pathogen damage per plant and species, as well as a floristic description of the understory of each of the four sites.
Damage per plant and association of damage types
For each of the collected leaves from the understory plants we estimated the percentage of area lost to herbivores and/or pathogens classifying the leaves into six categories of damage: 0 (0% of leaf area damaged), 1 (1–6% of leaf area damaged), 2 (6–12% of leaf area damaged), 3 (12–25% of leaf area damaged), 4 (25–50% of leaf area damaged), and 5 (50–100% of leaf area damaged). In the case of diseased leaves the categories of damage were assigned considering both the necrosed and surrounding area, which might have been discolored or with an otherwise coloration in the lamina adjacent to the necrosed area. This classification system ensured that low levels of damage per leaf (<25%), which were the predominant ones (Dirzo, 1987
), would not be lumped into a single category. The proportion of area damaged per leaf was assessed visually and an index of pathogen damage per plant, IP (Kremer and Unterstenhöfer, 1967
; Dirzo and Domínguez, 1995
) was obtained according to the following formula:
We described the symptoms of pathogen damage and analyzed the leaves to determine the type of damage association. The leaves from the plants were assigned to any of four damage types: (1) herbivory and pathogen damage on the same leaf, (2) pathogen damage alone, (3) herbivory alone, and (4) intact leaves.
Isolation of the causal agents of damage and inoculation experiments
To isolate the causal agents of the observed symptoms, leaf sections of the affected area (including a marginal healthy section of 5 mm width) were immersed in sodium hypochlorite (1%) for 2 min. These were then rinsed in sterile distilled water and placed in potato–dextrose–agar plates and incubated at 20°C (see López, 1981
). After fungal growth occurred, cultures were purified using single-spore isolates (see Booth, 1971
) or by transferring, several times, small portions of the culture medium including the advancing margin of the mycelia (see López, 1981
). Although no antibacterial agents were applied to the culture media, no bacteria associated with the leaf portions were detected. Fungal morphotypes were described, and when possible, identified (Barnett and Hunter, 1972
; Streets, 1978
). To assess whether the isolated fungi were effectively the causal agents of the symptoms and to know the role played by herbivory (experimentally simulated) on the establishment of pathogens, we carried out inoculation experiments, whereby healthy disinfected leaves of 40 plant species were inoculated with the isolated pathogens. These plant species were chosen because they were relatively abundant in the field and showed characteristic symptoms of damage by leaf-fungal pathogens. To carry out the inoculation of leaves with the fungal pathogens we selected 20 plants from each plant species, growing in the field, with at least five healthy leaves (i.e., without any kind of visible damage). The plants and their leaves were marked and each leaf disinfected with alcohol (70%) and inoculated with an inoculum suspension using four treatments: (1) simulated herbivory (by inflicting wounds or scrapes that mimic the characteristic type of damage of each species, followed by the application of inoculum on the damaged lamina) (N = 5 plants), (2) direct contact, consisting of direct application of inoculum suspension, without damage (N = 5 plants), (3) control direct contact consisting of direct application of sterile water instead of the inoculum suspension, without damage (N = 5 plants), and (4) control simulated herbivory consisting of simulated herbivory followed by the application of sterile water instead of the inoculum suspension (N = 5 plants each). Purified fungi for inoculation were grown on 20 mL of potato–dextrose–agar medium in 50-mL flasks. To carry out the inoculations, these flasks were filled with an additional 30 mL of sterile distilled water. The inoculum suspensions were produced by shaking and scraping, with a sterile needle, a mixture of mycelia and spores of the fully developed fungi. To apply the inocula, a sterile cotton ball was immersed in the flasks with the suspension. The cotton balls were then placed on the lamina of the leaves to be inoculated. In cases where more than one fungal morphotype was isolated from a single lesion, we prepared a suspension with sterile distilled water, mycelia, and spores from all the isolated fungal morphotypes. Following this, each plant was covered with a plastic bag for 24 h to increase humidity and to avoid the inoculum from being washed away by rainfall. Plants were inspected daily, up to 15 d, until development of any disease symptom occurred. Once disease symptoms were observed, fungi were isolated and purified, as described above, to compare with those originally inoculated.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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2.0 (i.e., 6–12% of leaf area damaged).
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80% of the species had IP values <1.0 (including 20 undamaged species), and only one species (1.8%) had an IP >2.0. A species-level analysis showed that 38 plant species occurred in samples from both seasons of the year (Appendix 2). Taking into account only these plant species, 10.5% were healthy in the dry season while they were diseased in the rainy season, whereas 13.16% were healthy in the rainy season but diseased during the dry season. Furthermore, 15.79% of the species were healthy in both seasons. For these comparisons, a plant was considered as diseased if having one or more symptomatic leaves. The IP per plant, considering those plant species present and diseased in both seasons, was higher in 15 plant species during the dry season, while in 13 species it was higher in the rainy season. However Mann-Whitney U tests indicated that out of these 28 plant species differences were significant in only five of them (Fig. 2). Anthurium flexile, Anthurium penthaphyllum, and Diplazium lonchopyllum had higher IP values during the rainy season, while the IP values in Monstera acuminata and Thelypteris rhachiflexuosa were higher in the dry season (P < 0.05 in all cases).
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2 = 13.16; P < 0.01). In contrast, the numbers of symptomatic and nonsymptomatic leaves did not significantly vary between seasons (2 = 3.95; P > 0.05).
Considering the four predominant symptoms, at the leaf level (Fig. 3) we found that leaves were significantly more damaged by fungi causing small necrotic spots during the rainy season than during the dry season (2 = 45.42; P < 0.01). In contrast, leaves had significantly more blight during the dry season than during the rainy season (2 = 33.91; P < 0.01). The other two disease symptoms affected a similar proportion of leaves during both seasons.
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) and IP (Spearman Rho = 0.40; P > 0.60) or the percentage of plant species damaged (Spearman Rho = -0.20; P > 0.80) were statistically significant. Finally, our results do not show a consistent spatial variation in the levels of disease associated with the variations in the degree of shading of the studied sites. On the one hand, the percentage of symptomatic leaves did not vary among sites on a given season and, on the other, the highest values of IP corresponded to the site that ranked third in degree of shadiness.
Association of damage types
The analysis of types of damage (Table 2) indicated that a very low proportion (1.4%) of the leaves were damaged by fungi alone. Nevertheless, the percentage of leaves that bore damage of both pathogens and herbivores increased to nearly 43% of the total number of leaves. In contrast, 16% of the leaves were damaged by herbivory alone. This indicates that pathogen attack may be highly dependent on damage by herbivores, while herbivory can occur in the absence of pathogenic infection. A two-by-two contingency analysis of the association of pathogen damage (present/absent) and damage by herbivores (present/absent) using the number of leaves in each category (cf. Table 2) was highly significant (2 = 3956.88; P < 0.00001). In this contingency analysis there was a marked overrepresentation of the combination herbivory–pathogen and a marked underrepresentation of pathogen damage alone.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). The low incidence of cases of extensive pathogen damage in this forest (see also de la Cruz and Dirzo, 1987
; Dirzo, 1987
) suggests that our data may not be greatly underestimated. Nevertheless, a study directed to the long-term monitoring of pathogen damage and leaf persistence in individually marked leaves is needed to clarify this aspect. Although we do not know of any study assessing leaf-pathogen damage at the community level in any other tropical rain forest, it has been observed that many tropical plant species show leaf-spots, typically caused by fungi. For example, in Central Amazonian forests, associations between fungi and leaf-spots have been reported in seedlings of several Sapotaceous trees (Benítez-Malvido, García-Guzmán, and Kossmann-Ferraz, 1999
). Furthermore, Travers, Gilbert, and Perry (1998)
have also reported damage by a rust fungus in flowers and young leaves of Faramea occidentalis.
Our results showed that there was considerable variation in the levels of damage by pathogens among plant species. The most affected species included unrelated taxa such as Abuta panamensis (Menispermaceae) in the dry season, Astrocaryum mexicanum (Arecaceae) in the dry and rainy seasons, and Psychotria faxlucens (Rubiaceae) in the rainy season (cf. Appendix 2). On the other hand, many plant species were not attacked by pathogens, including several species represented by a few individuals, with few leaves, as well as a few abundant species (e.g., Cymbopetalum baillonii). The group of unattacked species included both unrelated taxa and congeneric species. High levels of damage in some species and the lack of damage in others may be explained by stochastic reasons (the probability of a pathogen of finding a suitable host as a function of its abundance), however, the high interspecific variations could be explained by variation in defensive mechanisms. Plant secondary metabolites have been found to be a determinant of leaf pathogenic infection in many plant species. For example, several phenolic compounds, and others, such as saponines, have been proposed as responsible for the resistance of plant tissues to a variety of pathogenic microorganisms (Agrios, 1997
). The role of secondary chemistry in explaining interspecific variation in pathogen damage warrants further study.
The seasonality present at Los Tuxtlas did not affect the incidence of leaf diseases. This suggests that the environmental conditions found in the understory of this forest are favorable for the establishment and growth of several pathogens throughout the year. Some studies (Dinoor, 1970
; Thrall and Jarosz, 1994
; García-Guzmán et al., 1996
) have shown that the interaction between host and pathogens has a very strong environmental component. Changes in specific physical factors may affect the host, the pathogen, or their interaction, by altering the germination of spores and growth of pathogens, as well as the germination, growth or susceptibility of host plants, disease expression, the survival of infected plants (Colhoun, 1973
; Agrios, 1997
), or behavior of vectors. One possible explanation for the lack of seasonal variation in disease incidence could be that leaf longevity is so extended that our sampling on a particular season could have included foliage infected in another season. Leaf longevity varies considerably among tropical species in the understory of neotropical forests (Barajas, 1998
), so this effect may have occurred in some species. This aspect warrants further investigation.
Temporal variation in disease incidence was only evident in two symptoms in Los Tuxtlas. We found that the percentage of leaves affected by small necrotic spots and blight varied between seasons. However, the pattern of variation of these two symptoms was not consistent. While the percentage of leaves affected by blight was higher during the dry season, the percentage of leaves affected by small necrotic spots was higher during the rainy season. Although this variation might have been the result of more suitable environmental conditions for the development and establishment of the causal agents of these particular symptoms, it is also possible that other factors might explain the seasonal variation observed in these two symptoms. For example, the apparently lower incidence of small necrotic spots in the dry season may have been the result of the extensive development of blight in that season thus obscuring the apparency of small necrotic spots.
Our study shows that there was not a spatial variation in the levels of damage by pathogens. This absence of variation may be explained by the similarity of the four study sites, which were representative of mature forest. Although the four sites represented a gradient of shading, probably the contrast among them was not as marked as that needed to cause significant contrasts in pathogen infection, such as that reported by Augspurger and Kelly (1984)
when comparing damping-off between mature forest and gaps. In addition, the diversity and density of host plants have been considered as important factors determining pathogen incidence and disease severity (Burdon and Chilvers, 1982
; Burdon, 1987
) and a number of examples, mainly in agricultural systems, have shown that the homogeneous spatial distribution and high densities of the host plants favor the spread and establishment of pathogenic microorganisms (Burdon and Chilvers, 1982
). In wild systems the number of studies is limited. However, the heterogeneity of these systems may result in pathogens being less likely to spread efficiently. For example, Carlsson and Elmqvist (1992)
reported that the occurrence of the systemic smut Microbotryum violaceum (= Ustilago violacea) was higher in larger and more dense populations of the host plant Silene dioica, while less dense populations remained healthy. Nevertheless, in our study the diversity of each site was not significantly related to the levels of damage by pathogens per plant or to the percentage of diseased plants.
Considering that some studies in natural wild systems with systemic (e.g., Augspurger and Kelly, 1984
; García-Guzmán et al., 1996
) and nonsystemic pathogens (Alexander, 1984
; Burdon et al., 1992
) have shown a positive relationship between host density and incidence of diseases, we suggest that in the understory of Los Tuxtlas the presence of high density single-species stands (e.g., seedling banks) (see Dirzo and Miranda, 1991
; Dirzo et al., 1992
), may render plants highly susceptible to infection due to an increased shading, moisture, and proximity of plant tissue available for plant pathogens and herbivorous insects. Thus, disease incidence in a large proportion of plants may take place.
In this forest, besides density, the positive relationship between herbivory and pathogen damage, as well as the high proportion of wound-dependent pathogens (inoculation experiments), suggests the presence of a high proportion of opportunistic or facultative parasitic fungi, unable to cause disease unless previous leaf wounding occurs. These factors could be increasing the chances of a plant becoming infected simply by virtue of the presence of diseased plants in high-density stands as well as herbivorous insects able to feed on different plant species. This could be an additional factor to explain why levels of infection were found to be consistently high among sites.
Plant pathogens can penetrate host tissues by a variety of means (Tarr, 1972
; Agrios, 1997
). However, in this study we obtained strong evidence suggesting that most of the pathogens causing leaf diseases in this forest required wounds or scrapes to penetrate the host tissues. Moreover, the inoculation experiments carried out in our study strongly suggest that these pathogens largely depend on the mechanical damage inflicted by herbivory and perhaps by other agents of physical damage, such as wind or water. This suggests that leaf pathogens in Los Tuxtlas seem to be dependent on an agent that is relatively common (although not necessarily predictable). Insects are known to be important agents of fungal, bacterial, and viral disease dissemination in many temperate and tropical agricultural systems. For example, Sphaceloma perseae, causal agent of scab in leaves of avocado, may be transmitted by insects (Carvalho, 1976
), and the blueberry shoestring virus is transmitted by the aphid Illinoia pepperi (Terhune et al., 1991
). However there is little evidence for the role insects play as pathogen-dispersal agents in tropical natural systems (see Benítez-Malvido, García-Guzmán, and Kossmann-Ferraz, 1999
, for an example). Alternatively, it could be argued that if the leaves of the understory plants are poorly defended (and/or have high quality for consumers) they could be attacked simultaneously by both insects and pathogens leading to an association like the one found in this study (P. D. Coley, personal communication, University of Utah). However, our inoculation experiments strongly support the argument of pathogen dependence on herbivore damage.
The pathogens affecting these species were fungi that caused discrete lesions that individually may have little noticeable effect on host fitness. Other studies in temperate forests have shown that nonsystemic leaf pathogens, such as the ones found in our study, have limited or no discernible effect on their hosts (Burdon, 1993
). However, when plants are severely diseased, foliar pathogens can reduce survivorship, reproduction, growth, and competitive ability of infected plants (Jarosz and Davleos, 1995
). Nevertheless, the combined effects of herbivory and pathogen damage found in a high proportion of the surveyed plants may affect the performance of the host plants in this forest by reducing the photosynthetic area. This three-way interaction is an aspect that warrants further study.
The interplay between biotic and abiotic factors is vital in determining the intensity of host–pathogen interactions and their long-term consequences. It has been suggested that pathogens that cause local leaf lesions are characterized by high levels of spatial and temporal variability, often related to habitat, weather, or climatic variables (Jarosz and Davelos, 1995
). This has been particularly evident in some associations involving local lesion diseases, such as wild barley infected by the powdery mildew Erysiphe graminis (Dinoor and Eshed, 1990
) and Linum marginale infected by the rust Melampsora lini (Jarosz and Burdon, 1992
). In these cases it was found that disease incidence was highly variable both spatially and temporally. The need for specific environmental conditions and the susceptibility of hosts seem to be primarily responsible for the observed variability (Jarosz and Davelos, 1995
). However, more studies are needed to determine whether this is also the case for tropical systems such as Los Tuxtlas, where climatic conditions remain more or less constant throughout the year.
Disease can affect plant fitness in a myriad of ways, however more detailed studies are needed to determine the impact of leaf-fungal pathogens at the population and community dynamics of tropical systems (see Augspurger and Kelly, 1984
). Our results suggest that the study of plant–pathogen interactions constitutes an area of potential interest in the field of the biotic interactions in tropical natural systems and highlights the role of herbivory in the ecology of plant diseases in natural communities. Furthermore, our study places tropical herbivory in another perspective, whereby phytophagous insects are not to be seen only as agents of leaf tissue removal, but as agents of disease facilitation and/or dispersal.
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FOOTNOTES |
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2 Author for reprint requests (e-mail: mggarcia{at}miranda.ecologia.unam.mx
).
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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