BIOMASS DISTRIBUTION IN DECLINING SACRED-FIR SEEDLINGS

Miguel Ángel López-López, Alejandro Velázquez-Martínez, Juan Acosta-Montoya and Elizabeth Estañol-Botello

Miguel Ángel López López. Agronomist, Universidad Autónoma Chapingo (UACh), México. M.Sc., Colegio de Postgraduados, México. Ph.D., Colorado State University, USA. Researcher Professor, Colegio de Postgraduados, Montecillo, México. e-mail: lopezma@colpos.mx

Alejandro Velázquez Martínez. Agronomist, UACh, México. M.Sc., Colegio de Postgraduados, México. Ph.D., Oregon State University, USA. Researcher Professor, Colegio de Postgraduados, Montecillo, México. Address: Km 36.5, Carretera México-Texcoco. Montecillo, Texcoco, Estado de México. México 56230. e-mail: alejvela@colpos.mx

Juan Acosta Montoya. Agronomist, UACh, México. Hydrological Services Promoter, Comisión Nacional Forestal, Morelia, Michoacan, México. e-mail: jacostam@hotmail.com

Elizabeth Estañol-Botello. Biologist, Universidad Nacional Autónoma de México. M.Sc., Colegio de Postgraduados, México. D.Sc., Colegio de Postgraduados, Mexico. e-mail: estanol@colpos.mx.

SUMMARY

In the forests located west and southwest of Mexico City, decline of sacred-fir Abies religiosa (H.B.K.) Schl. et Cham. has been observed for the past 25 years. Characterization of the phenomenon from different viewpoints is important if knowledge of the problem is to be increased and viable solutions pursued. For this reason, changes in biomass allocation patterns, as a consequence of decline in 7-year-old seedlings were investigated. A completely randomized experiment with three degrees of damage as treatments: slight, intermediate and severe; and eight replicates per treatment was established. The biomass of the seedling components was significantly reduced as the damage increased. Root was the most affected organ followed by twigs. However, twigs accumulated biomass through time producing an imbalance between aboveground and root biomass. Even though this imbalance is offset by leaf fall, this brings about a further reduction in the amount of carbon fixed.

DISTRIBUCIÓN DE BIOMASA EN PLÁNTULAS DE OYAMEL EN DECLINACIÓN

RESUMEN

En los bosques localizados en el oeste y suroeste de la Ciudad de México se ha observado una declinación del oyamel Abies religiosa (H.B.K.) Schl. et Cham. durante los últimos 25 años. La caracterización de este fenómeno desde diferentes puntos de vista es importante si se pretende incrementar el conocimiento sobre el problema y proponer soluciones viables. Por esta razón se estudiaron los cambios en los patrones de distribución de biomasa en plántulas de 7 años de edad, como resultado de la declinación. Se estableció un experimento completamente al azar con tres niveles de daño como tratamientos: ligero, intermedio y severo, y ocho repeticiones por tratamiento. La biomasa de los componentes de las plántulas se redujo significativamente a medida que se incrementó el daño. La raíz fue el componente más afectado, seguido de las ramillas. Sin embargo, estas últimas acumularon biomasa con el tiempo, produciendo un desbalance entre la biomasa aérea y subterránea. Aun cuando este desbalance se compensa por la caída de follaje, trae como consecuencia una reducción de la cantidad de carbono fijado.

DECLÍNIO DA BIOMASSA EM MUDAS DE "SACRED-FIR" PLÂNTULAS)

RESUMO

Nos bosques localizados no Sudoeste da Cidade do México tem-se observado uma declinação do oyamel Abies religiosa (H.B.K.) Schl. et Cham. Durante os últimos 25 anos. A caracterização deste fenômeno desde diferentes pontos de vista é importante si se pretende incrementar o conhecimento sobre o problema e propor soluções viáveis. Por esta razão se estudaram as mudanças nos padrões de distribuição de biomassa em plântulas de 7 anos de idade, como resultado da declinação. Estabeleceu-se um experimento completamente aleatório com três níveis de dano como tratamentos: ligeiro, intermediário e severo, e oito repetições por tratamento. A biomassa dos componentes das plântulas se reduziu significativamente a medida que se incrementou o dano. A raíz foi o componente mais afetado, seguido dos galhos. No entanto, estas últimas acumularam biomassa com o tempo, produzindo um desbalanço entre a biomassa aérea e subterrânea. Mesmo quando este desbalanço se compensa pela queda da folhagem, traz como consequência uma redução da quantidade de carbono fixado.

KEYWORDS / Abies religiosa / Biomass Distribution / Forest Decline / Seedling /

Received: 04/07/2005. Modified: 04/10/2006. Accepted: 04/25/2006.

Introduction

The term "forest decline" is associated with a broad range of symptoms, including scarcity and discoloration of foliage, reduction in leaf size, mortality of branches, reduction in growth rates, mortality of trees, and poor regeneration of affected species, among others (Tingey et al., 1976; Oren et al., 1989; Hernández-Tejeda et al., 2001). In the early 80s, De la Isla de Bauer and co-workers first reported the presence of symptoms of forest decline at the National Park "Desierto de los Leones" (DL) southwest of Mexico City (López, 1996), suggesting high tropospheric ozone as a possible causal factor. To date, several studies have attempted to understand and determine the causal factors of decline and several authors have pointed out to multiple causes including air pollution, pests and diseases, water extraction, poor forest management practices, and natural succession (Sierra et al., 1988; Alvarado et al., 1993). Nowadays, there is a general consensus that a primary cause of sacred-fir decline may be air pollution, especially atmospheric ozone originating in Mexico City that is transported towards the southw est of the Valley of Mexico (Hernández, 1984; Ciesla and Macías, 1987; Cibrián, 1989; López, 1996, 1997; Alvarado-Rosales and Hernández-Tejeda, 2002).

Although no specific studies on ozone as a causal factor of decline of sacred-fir have been carried out, available data show that ozone is one of the air pollutants that most frequently exceed the air quality standards in the southwest of the Valley of Mexico (Bravo-Álvarez and Torres-Jardón, 2002). López (1997) found that pot grown sacred-fir seedlings developed symptoms like those shown by adult declining trees when they grew in the DL, but not when they grew in a site under similar conditions in the east of the Valley of Mexico, regardless of soil origin. This finding led to conclude that air at DL is responsible for the decline syndrome in sacred-fir seedlings.

The most common visible symptom observed in declining forests is needle chlorosis, which may be due to the loss of chlorophyll as a consequence of high ozone concentrations. Miller et al. (1963) found that the treatment of Pinus ponderosa needles with 0.5ppm ozone during 9-18 days in the field led to the development of chlorotic mottling of leaves. Additionally, the chlorophyll content of leaves exposed to ozone for 18 days was generally lower than that of control plants. López and Rivera (1995) suggested that destruction of chlorophyll is likely determined by the need for nutrients in the new foliage, since it is the one-year-old or older foliage that shows this symptom. Additionally, chlorosis of existing foliage begins to appear early in the growing season, when new foliage starts to grow (López, 1996). Consistent with the previous statements, Nambiar and Fife (1987) reported that chlorosis of old foliage did not appear when they suppressed the new growth. This suggests that chlorosis is linked to source-sink relationships within the plant.

Since retranslocation of a mineral is generally coupled with movement of other nutrients (Saur et al., 2000; Salifu and Timmer, 2001), it was expected that such source-sink relationships impact not only mineral nutrients but also carbon compounds, thus altering biomass distribution patterns within seedlings.

Changes in carbon distribution patterns within trees may derive from different types of stress such as moisture stress (McMillin and Wagner, 1995), shading (King, 1997), high soil acidification (Liu and Tyree, 1997) and air pollution (McLaughlin et al., 1982). Those changes may be considered as a strategy of plants to reach the appropriate balance among plant components according to situations imposed by stressing factors. In general, species with high growth rates can alter carbon distribution patterns in response to stress more easily than those with low growth rates (Laurence et al., 1994). These changes are generally due to changes in photosynthate metabolism (McLaughlin et al., 1982). Hogsett et al. (1985), for example, found a reduction in growth of Pinus elliotti when the ozone concentration was experimentally increased; however, root growth was more drastically reduced.

If stressing factors alter the biomass distribution patterns within declining perennial seedlings or trees, these trees are expected to develop abnormal morphological and/or physiological characteristics in the long run. This is especially true if the stressing factors are long lasting, which will likely cause the effects of the changed patterns of biomass distribution to become cumulative through time.

Based on the previous information, it is hypothesized that biomass distribution patterns in sacred-fir seedlings change with varying degrees of decline. Accordingly, the purpose of this study was to analyze and discuss the behavior of the biomass distribution of Abies religiosa seedlings under different degrees of damage, and to determine which plant components (foliage, stem-and-branch wood and root) and component ratios are more sensitive to the processes of decline.

Materials and Methods

This study was carried out in an Abies religiosa plantation of ~1ha established in 1992 at the De las Cruces Mountains, Huixquilucan, State of Mexico. In this site, the former natural sacred-fir forest was degraded by both illegal harvesting and decline. The plantation was established by Protectora de Bosques (PROBOSQUE) using seedlings produced in a nursery at Metepec, State of Mexico. Damaged seedlings at the time the experiment was carried out accounted for approximately 70% and were rather randomly distributed throughout the plantation area.

The site’s coordinates are 19º17'08''N and 99º19'16''W. The site is located approximately 15km southwest of Mexico City (Figure 1) and 6.5km from the so called Cemetery I at the DL, where severe decline has appeared. The elevation of the plantation site ranges from 3250 to 3300m. The mean slope is 30% with a northwest aspect. Mean temperature is between 8 and 10ºC, and annual precipitation is between 1200 and 1500mm. According to Köppen’s climate classification, modified by García (1973), the climate in the zone is C(e), that is, cold temperate, humid with benign winters.

During a trip throughout the plantation on March 13th, 1997, a total of seventy-five 7-year-old (2 years in the nursery and 5 years in the field) seedlings were selected. The selection of seedlings was based on general visual symptoms including chlorosis, reddening and/or leaf fall. During this stage, seedlings were identified and labeled visually as being healthy, severely damaged or with an intermediate level of damage. Thereafter, the seedlings were further evaluated by using photographic scales for chlorosis and needle loss that were previously designed and tested for its discriminatory capacity by López et al. (1995). This evaluation was based on a sample of internodes from each seedling which included 20% of the 2-year-old internodes. After estimating the index of damage (ID) for each seedling, all 75 seedlings were sorted in ascending order according to such ID. The seedling groups were obtained by selecting the 8 seedlings with the lowest, 8 seedlings with intermediate and 8 seedlings with the highest IDs. These groups were considered as the source of variation or treatments, while 8 seedlings within each group were the replicates. Average dimensions of the seedlings finally selected are shown in Table I.

The photographic scale used to evaluate seedling damage produces an ID for a group of internodes (sample of internodes within a seedling), based on the degree of chlorosis, reddening of foliage and foliage loss, although in our study only chlorosis and needle loss were included since reddening is much less common at the study site. The degree of damage for an internode is obtained by comparing it with internodes shown in a pre-designed photograph, in which the healthiest internode was assigned a value of 0, while the most damaged one was assigned a value of 2 for chlorosis and reddening and 3 for needle loss.

The calculation of the ID for a group of internodes was done by using the equation (López et al., 1995)

ID = (S(i×n_i)×100)/(n×MDD)

where i: degree of damage for a given internode (according to a photographic scale), ni: number of internodes with a degree of damage i, n: total number of internodes in the sample or seedling, and MDD: maximum degree of damage in the photographic scale.

Before using the ANOVA procedure of SAS to contrast the groups of seedlings, the Bartlett and Shapiro-Wilk tests were used to test the data for variance homogeneity and normality, respectively.

On March 25^th, 1997, the three groups of seedlings selected were harvested including roots. The roots were rinsed to eliminate soil particles. The biomass was separated into aboveground parts and roots. Aboveground biomass was in turn separated into its components (foliage and twigs) and foliage was separated based on age. The materials were oven-dried at 70ºC until constant weight and the weights were recorded. Using the ANOVA procedure of SAS, comparisons between the treatments were carried out according to a completely randomized experimental design.

Results and Discussion

Premature abscission of older foliage is a common symptom of tree decline in the zone under study (López, 1993). This symptom makes it difficult to use old (>1 year old) foliage in carbon distribution studies, unless the amount of foliar biomass abscised has been measured. However, the use of healthy foliar biomass such as that produced during the previous growing season may be useful to estimate the amount of carbon devoted to the production of foliage. In the case of wood, the last twigs produced may also represent an important amount of the carbon devoted to wood production; however, the wood added to older shoots as secondary growth may also account for an important proportion of the wood generated in a year. Nevertheless, the separation of the woody tissue by year in older shoots is a difficult task that would require long-term studies.

As shown in Table II, the amount of carbon devoted to production of foliage in 1996 was significantly reduced with symptom severity. Leaf production in the seedlings with intermediate damage was only about 61% (a 39% decrease) of that in the healthiest seedlings, while production of needles in the most damaged seedlings was only 39% of that in the healthiest seedlings.

Similarly, new twig production was reduced as damage increased (Table II). Wood biomass in the new shoots of intermediate and severely damaged seedlings was 70 and 48% (30 and 52% decrease) of that in the least damaged seedlings, respectively. The same tendency is shown by the total root biomass, which decreased by 28 and 58% in intermediate and severely damaged seedlings, respectively.

These trends imply that total biomass increment was reduced by the symptoms of decline by roughly 50%. This overall reduction is likely to be primarily due to a reduction in size of the photosynthetic biomass of damaged seedlings, since total foliar biomass was reduced by the damage by around 70% (Table II).

The overall reduction in seedling growth negatively affects seedling vigor and performance, and makes it difficult to regenerate the decline-affected sites with the declining species since high symptom-related mortality rates occur through the plantation lifespan. However, the induction of differential changes in size among seedling organs may have more important implications on seedling performance. Biomass accumulation in different organs with respect to total seedling biomass (Figure 2) indicates that whereas foliar biomass decreases (p<0.046) and root biomass tends to decrease (not significantly, p<0.274) with increasing damage, wood biomass accumulation significantly increases (p<0.011). This implies that an imbalance of biomass between the different organs arises from the presence of decline, which can bring about further stress in the seedlings.

Apparently, the balance between root biomass and leaf biomass is maintained regardless of the degree of damage (Table III). However, if it is considered that decreased foliar biomass in the most damaged trees is due, to a large extent, to leaf fall (Alvarado et al., 1993), then it is clear that the root is the organ receiving the least amount of carbohydrates, and leaf fall may be just a strategy of declining plants to maintain the balance between water-absorbing (roots) and transpiring (leaves) organs. This pattern of decrease of carbon allocation in roots was also found in Populus tremuloides by Coleman et al. (1996) who also determined that root respiration rates remained the same in ozone-exposed seedlings as in control plants. Their finding further indicated that the reduced root biomass in damaged seedlings is due to a decreased carbon allocation to this organ instead of an increased root respiration. Ardö (1998) and Grulke et al. (2001) stated that atmospheric nitrogen inputs (one of the possible causes of forest decline) triggers an imbalance of the tree aboveground/root ratio in Pinus ponderosa Dougl. ex Laws. by disproportionately increasing aboveground biomass.

Unlike leaves, shoot wood is accumulated and maintained in the seedling regardless of the degree of damage. If this accumulation of biomass were not offset by leaf fall, the root/aboveground-biomass ratio would be drastically decreased. Again, this may imply that leaf fall is necessary to maintain the balance among the compartments of the seedlings. Wood accumulation in shoots also generated a significant (p<0.05) increase in the wood/foliage ratio (Table III) with increasing damage. This imbalance may be especially important during the seedling stage, since live wood accumulation represents increased seedling respiration at the time that photosynthetic biomass is reduced. Thus, a decreasing trend of net carbon fixation is expected to be triggered by decline, which eventually could lead to premature tree death (García et al., 1998).

Conclusions

Biomass accumulation in roots, twigs and leaves significantly decreases as the symptoms of decline become more severe. However, this reduction is not proportional in all seedling components. Root biomass is the most strongly affected, followed by twigs and leaf biomass. Cumulative shoot wood growth in seedlings would be expected to bring about a strong imbalance in terms of biomass between aboveground tissues and roots. However, leaf fall offsets this imbalance, although it also decreases carbon fixation, which may also be negatively impacted by the respiration of the disproportionate shoot wood accumulation. These dynamics are expected to lead to tree mortality early in the development of declining A. religiosa stands, thus making it difficult to get affected stands to regenerate.

ACKNOWLEDGeMENTS

The authors thank Dave Perry, and Colegio de Postgraduados for allowing to use the facilities needed for both field and laboratory studies.

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