Interciencia ISSN: 0378-1844 [email protected] Asociación Interciencia Venezuela

López López, Miguel Ángel; Velázquez Martínez, Alejandro; Acosta Montoya, Juan; Estañol-Botello, Elizabeth Biomass distribution in declining sacred- seedlings Interciencia, vol. 31, núm. 6, junio, 2006, pp. 451-455 Asociación Interciencia Caracas, Venezuela

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How to cite Complete issue Scientific Information System More information about this article Network of Scientific Journals from Latin America, the Caribbean, Spain and Portugal Journal's homepage in redalyc.org Non-profit academic project, developed under the open access initiative BIOMASS DISTRIBUTION IN DECLINING SACRED-FIR SEEDLINGS

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

SUMMARY

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

RESUMEN

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

Introduction de los Leones” (DL) south- especially atmospheric ozone Jardón, 2002). López (1997) west of Mexico City (López, originating in Mexico City found that pot grown sacred- The term “forest decline” is 1996), suggesting high tropo- that is transported towards the fir seedlings developed symp- associated with a broad range spheric ozone as a possible southw est of the Valley of toms like those shown by of symptoms, including scar- causal factor. To date, several Mexico (Hernández, 1984; adult declining when city and discoloration of foli- studies have attempted to un- Ciesla and Macías, 1987; they grew in the DL, but not age, reduction in leaf size, derstand and determine the Cibrián, 1989; López, 1996, when they grew in a site un- mortality of branches, reduc- causal factors of decline and 1997; Alvarado-Rosales and der similar conditions in the tion in growth rates, mortality several authors have pointed Hernández-Tejeda, 2002). east of the Valley of Mexico, of trees, and poor regenera- out to multiple causes includ- Although no specific stud- regardless of soil origin. This tion of affected species, ing air pollution, pests and ies on ozone as a causal fac- finding led to conclude that among others (Tingey et al., diseases, water extraction, tor of decline of sacred-fir air at DL is responsible for 1976; Oren et al., 1989; poor forest management prac- have been carried out, avail- the decline syndrome in sa- Hernández-Tejeda et al., tices, and natural succession able data show that ozone is cred-fir seedlings. 2001). In the early 80s, De la (Sierra et al., 1988; Alvarado one of the air pollutants that The most common visible Isla de Bauer and co-workers et al., 1993). Nowadays, there most frequently exceed the air symptom observed in declin- first reported the presence of is a general consensus that a quality standards in the south- ing forests is needle chlorosis, symptoms of forest decline at primary cause of sacred-fir west of the Valley of Mexico which may be due to the loss the National Park “Desierto decline may be air pollution, (Bravo-Álvarez and Torres- of chlorophyll as a conse-

KEYWORDS / Abies religiosa / Biomass Distribution / Forest Decline / Seedling / Received: 04/07/2005. Modified: 04/10/2006. Accepted: 04/25/2006.

Miguel Ángel López López. Alejandro Velázquez Martínez. de México. México 56230. e- Elizabeth Estañol-Botello. Biolo- Agronomist, Universidad Au- Agronomist, UACh, México. mail: [email protected] gist, Universidad Nacional tónoma Chapingo (UACh), M.Sc., Colegio de Postgra- Juan Acosta Montoya. Agrono- Autónoma de México. M.Sc., México. M.Sc., Colegio de duados, México. Ph.D., Or- mist, UACh, México. Hydro- Colegio de Postgraduados, Postgraduados, México. Ph.D., egon State University, USA. logical Services Promoter, México. D.Sc., Colegio de Colorado State University, Researcher Professor, Colegio Comisión Nacional Forestal, Postgraduados, Mexico. e-mail: USA. Researcher Professor, de Postgraduados, Montecillo, Morelia, Michoacan, México. [email protected]. Colegio de Postgraduados, México. Address: Km 36.5, e-mail: [email protected] Montecillo, México. e-mail: Carretera México-Texcoco. [email protected] Montecillo, Texcoco, Estado

JUN 2006, VOL. 31 Nº 6 0378-1844/06/06/451-05 $ 3.00/0 451 RESUMO

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

quence of high ozone concen- (McLaughlin et al., 1982). branch wood and trations. Miller et al. (1963) Those changes may be con- root) and compo- found that the treatment of sidered as a strategy of nent ratios are Pinus ponderosa needles with to reach the appropriate bal- more sensitive to 0.5ppm ozone during 9-18 ance among components the processes of days in the field led to the according to situations im- decline. development of chlorotic mot- posed by stressing factors. In tling of . Additionally, general, species with high Materials and the chlorophyll content of growth rates can alter carbon Methods leaves exposed to ozone for distribution patterns in re- 18 days was generally lower sponse to stress more easily This study was than that of control plants. than those with low growth carried out in an López and Rivera (1995) sug- rates (Laurence et al., 1994). Abies religiosa gested that destruction of These changes are generally plantation of ~1ha chlorophyll is likely deter- due to changes in photosyn- established in mined by the need for nutri- thate metabolism (McLaughlin 1992 at the De las Figure 1. Location of the study site in the central ents in the new foliage, since et al., 1982). Hogsett et al. Cruces Mountains, part of the municipality of Huixquilucan, Estado de it is the one-year-old or older (1985), for example, found a Huixquilucan, México. foliage that shows this symp- reduction in growth of Pinus . tom. Additionally, chlorosis of elliotti when the ozone con- In this site, the former natural zone is C(e), that is, cold existing foliage begins to ap- centration was experimentally sacred-fir forest was degraded temperate, humid with benign pear early in the growing sea- increased; however, root by both illegal harvesting and winters. son, when new foliage starts growth was more drastically decline. The plantation was During a trip throughout the to grow (López, 1996). Con- reduced. established by Protectora de plantation on March 13th, 1997, sistent with the previous state- If stressing factors alter the Bosques (PROBOSQUE) us- a total of seventy-five 7-year- ments, Nambiar and Fife biomass distribution patterns ing seedlings produced in a old (2 years in the nursery and (1987) reported that chlorosis within declining perennial nursery at Metepec, State of 5 years in the field) seedlings of old foliage did not appear seedlings or trees, these trees Mexico. Damaged seedlings were selected. The selection of when they suppressed the new are expected to develop ab- at the time the experiment seedlings was based on general growth. This suggests that normal morphological and/or was carried out accounted for visual symptoms including chlorosis is linked to source- physiological characteristics in approximately 70% and were chlorosis, reddening and/or leaf sink relationships within the the long run. This is espe- rather randomly distributed fall. During this stage, - plant. cially true if the stressing fac- throughout the plantation area. lings were identified and la- Since retranslocation of a tors are long lasting, which The site’s coordinates are beled visually as being healthy, mineral is generally coupled will likely cause the effects of 19º17'08''N and 99º19'16''W. severely damaged or with an with movement of other nutri- the changed patterns of bio- The site is located approxi- intermediate level of damage. ents (Saur et al., 2000; Salifu mass distribution to become mately 15km southwest of Thereafter, the seedlings were and Timmer, 2001), it was cumulative through time. Mexico City (Figure 1) and further evaluated by using pho- expected that such source-sink Based on the previous in- 6.5km from the so called tographic scales for chlorosis relationships impact not only formation, it is hypothesized Cemetery I at the DL, where and needle loss that were pre- mineral nutrients but also car- that biomass distribution pat- severe decline has appeared. viously designed and tested for bon compounds, thus altering terns in sacred-fir seedlings The elevation of the planta- its discriminatory capacity by biomass distribution patterns change with varying degrees tion site ranges from 3250 to López et al. (1995). This evalu- within seedlings. of decline. Accordingly, the 3300m. The mean slope is ation was based on a sample of Changes in carbon distribu- purpose of this study was to 30% with a northwest aspect. internodes from each seedling tion patterns within trees may analyze and discuss the be- Mean temperature is between which included 20% of the 2- derive from different types of havior of the biomass distri- 8 and 10ºC, and annual pre- year-old internodes. After esti- stress such as moisture stress bution of Abies religiosa cipitation is between 1200 mating the index of damage (McMillin and Wagner, 1995), seedlings under different de- and 1500mm. According to (ID) for each seedling, all 75 shading (King, 1997), high grees of damage, and to de- Köppen’s climate classifica- seedlings were sorted in as- soil acidification (Liu and termine which plant compo- tion, modified by García cending order according to Tyree, 1997) and air pollution nents (foliage, stem-and- (1973), the climate in the such ID. The seedling groups

452 JUN 2006, VOL. 31 Nº 6 TABLE I it difficult to use old (>1 year and 58% in intermediate and AVERAGE DIMENSIONS OF THE SEEDLINGS USED old) foliage in carbon distri- severely damaged seedlings, WITHIN EACH DAMAGE CATEGORY bution studies, unless the respectively. amount of foliar biomass ab- These trends imply that to- Damage category Height (cm) Root collar diameter (cm) scised has been measured. tal biomass increment was re- 0 73.2 ±4.43 1.7 ±0.25 However, the use of healthy duced by the symptoms of 1 69.3 ±5.47 1.4 ±0.30 foliar biomass such as that decline by roughly 50%. This 2 65.7 ±4.07 1.3 ±0.32 produced during the previous overall reduction is likely to growing season may be useful be primarily due to a reduc- to estimate the amount of car- tion in size of the photosyn- were obtained by selecting the to a photographic scale), ni: bon devoted to the production thetic biomass of damaged 8 seedlings with the lowest, 8 number of internodes with a of foliage. In the case of seedlings, since total foliar seedlings with intermediate and degree of damage i, n: total wood, the last twigs produced biomass was reduced by the 8 seedlings with the highest number of internodes in the may also represent an impor- damage by around 70% IDs. These groups were consid- sample or seedling, and MDD: tant amount of the carbon de- (Table II). ered as the source of variation maximum degree of damage voted to wood production; The overall reduction in or treatments, while 8 seedlings in the photographic scale. however, the wood added to seedling growth negatively af- within each group were the Before using the ANOVA older shoots as secondary fects seedling vigor and per- replicates. Average dimensions procedure of SAS to contrast growth may also account for formance, and makes it diffi- of the seedlings finally selected the groups of seedlings, the an important proportion of the cult to regenerate the decline- are shown in Table I. Bartlett and Shapiro-Wilk tests wood generated in a year. affected sites with the declin- The photographic scale used were used to test the data for Nevertheless, the separation ing species since high symp- to evaluate seedling damage variance homogeneity and nor- of the woody tissue by year tom-related mortality rates oc- produces an ID for a group of mality, respectively. in older shoots is a difficult cur through the plantation internodes (sample of intern- On March 25th, 1997, the task that would require long- lifespan. However, the induc- odes within a seedling), based three groups of seedlings se- term studies. tion of differential changes in on the degree of chlorosis, red- lected were harvested includ- As shown in Table II, the size among seedling organs dening of foliage and foliage ing roots. The roots were amount of carbon devoted to may have more important im- loss, although in our study only rinsed to eliminate soil par- production of foliage in 1996 plications on seedling perfor- chlorosis and needle loss were ticles. The biomass was sepa- was significantly reduced with mance. Biomass accumulation included since reddening is rated into aboveground parts symptom severity. Leaf pro- in different organs with re- much less common at the and roots. Aboveground bio- duction in the seedlings with spect to total seedling bio- study site. The degree of dam- mass was in turn separated intermediate damage was only mass (Figure 2) indicates that age for an internode is obtained into its components (foliage about 61% (a 39% decrease) whereas foliar biomass de- by comparing it with intern- and twigs) and foliage was of that in the healthiest seed- creases (p<0.046) and root odes shown in a pre-designed separated based on age. The lings, while production of biomass tends to decrease photograph, in which the materials were oven-dried at needles in the most damaged (not significantly, p<0.274) healthiest internode was as- 70ºC until constant weight and seedlings was only 39% of with increasing damage, wood signed a value of 0, while the the weights were recorded. that in the healthiest seed- biomass accumulation signifi- most damaged one was as- Using the ANOVA procedure lings. cantly increases (p<0.011). signed a value of 2 for chloro- of SAS, comparisons between Similarly, new twig produc- This implies that an imbal- sis and reddening and 3 for the treatments were carried out tion was reduced as damage ance of biomass between the needle loss. according to a completely ran- increased (Table II). Wood different organs arises from The calculation of the ID for domized experimental design. biomass in the new shoots of the presence of decline, a group of internodes was done intermediate and severely which can bring about further by using the equation (López Results and Discussion damaged seedlings was 70 stress in the seedlings. et al., 1995) and 48% (30 and 52% de- Apparently, the balance be- Premature abscission of crease) of that in the least tween root biomass and leaf Σ ID = ( (i×ni)×100)/(n×MDD) older foliage is a common damaged seedlings, respec- biomass is maintained regard- symptom of decline in tively. The same tendency is less of the degree of damage where i: degree of damage for the zone under study (López, shown by the total root bio- (Table III). However, if it is a given internode (according 1993). This symptom makes mass, which decreased by 28 considered that decreased fo-

TABLE II EFFECTS OF DAMAGE ON SEEDLING COMPARTMENT BIOMASS ID FB 1996 TFB WB - 1996 WB 1996 TWB TRB Reduction Reduction Reduction Reduction Reduction Reduction (g) (%) (g) (%) (g) (%) (g) (%) (g) (%) (g) (%) 0 28.23 ±2.15a 0.0 39.83 ±2.79a 0.0 62.50 ±3.93a 0.0 10.92 ±0.35a 0.0 73.42 ±3.94a 0.0 29.35 ±2.99a 0.0 1 16.75 ±2.00b 40.7 21.57 ±2.58b 45.8 41.63 ±3.98b 33.4 7.57 ±0.37b 30.7 49.20 ±4.03b 34.0 21.09 ±2.78b 28.1 2 10.97 ±1.32b 61.1 12.23 ±2.04c 69.3 34.33 ±2.28c 45.1 5.29 ±0.41b 51.6 39.61 ±2.58c 46.1 12.23 ±2.74b 58.3 ID: Index of damage, FB 1996: Foliar biomass 1996, TFB: Total foliar biomass, WB – 1996: Wood biomass produced before 1996, WB 1996: Wood biomass 1996, TWB: Total wood biomass, TRB: Total root biomass. 0= Slight damage, 1=Intermediate damage, 2=Severe damage. For a given type of tissue, biomass values among damage severity classes with the same letter are not statistically different.

JUN 2006, VOL. 31 Nº 6 453 gered by decline, which even- tropolitan Area. In Fenn ME, tually could lead to premature LI de Bauer, Hernández-Tejeda T (Eds.) Urban air pollution tree death (García et al., and forests. Resources at risk 1998). in the Mexico City air basin. Springer. New York, USA. pp. Conclusions 121-159. Cibrian TD (1989) Air pollution Biomass accumulation in and forest decline near Mexico City. Env. Monit. Assess. 12: roots, twigs and leaves sig- 49-58. nificantly decreases as the Ciesla WM, Macías SJE (1987) symptoms of decline become Desierto de los Leones: A for- more severe. However, this est in crisis. Amer. For. 93: 29- reduction is not proportional 31, 72-74. in all seedling components. Coleman MD, Dickson RE, Root biomass is the most Isebrands JG, Karnosky DF strongly affected, followed by (1996) Root growth and physi- ology of potted and field- Figure 2. Biomass distribution with respect to total biomass in relatively twigs and leaf biomass. Cu- grown trembling aspen ex- healthy (0), moderately damaged (1), and severely damaged (2) Abies mulative shoot wood growth posed to tropospheric ozone. religiosa seedlings. For a given type of tissue, biomass values among dam- in seedlings would be ex- Tree Physiol. 16: 145-152. age severity classes with the same letter are not statistically different. pected to bring about a strong García E (1973) Modificaciones al imbalance in terms of bio- sistema de clasificación cli- nd mass between aboveground mática. 2 ed. Instituto de liar biomass in the most dam- of the tree aboveground/root Geografía. UNAM. México. aged trees is due, to a large ratio in Pinus ponderosa tissues and roots. However, 446 pp. extent, to leaf fall (Alvarado Dougl. ex Laws. by dispro- leaf fall offsets this imbal- García BRM, López LMA, Ve- et al., 1993), then it is clear portionately increasing above- ance, although it also de- lázquez MA, Pérez MJ (1998) that the root is the organ re- ground biomass. creases carbon fixation, which Mycorrhizal and saprotrophic ceiving the least amount of Unlike leaves, shoot wood may also be negatively im- macrofungi in declining sa- pacted by the respiration of cred-fir stands. Micol. Neotrop. carbohydrates, and leaf fall is accumulated and main- Apl. 11: 9-21. the disproportionate shoot may be just a strategy of de- tained in the seedling regard- Grulke NE, Andersen CP, Hogsett clining plants to maintain the less of the degree of damage. wood accumulation. These WE (2001) Seasonal changes balance between water-ab- If this accumulation of bio- dynamics are expected to lead in above- and belowground sorbing (roots) and transpiring mass were not offset by leaf to tree mortality early in the carbohydrate concentrations of (leaves) organs. This pattern fall, the root/aboveground-bio- development of declining A. ponderosa pine along a pollu- religiosa stands, thus making tion gradient. Tree Physiol. 21: of decrease of carbon alloca- mass ratio would be drasti- 173-181. tion in roots was also found cally decreased. Again, this it difficult to get affected stands to regenerate. Hernández TT (1984) Efecto de los in Populus tremuloides by may imply that leaf fall is gases oxidantes sobre algunas Coleman et al. (1996) who necessary to maintain the bal- especies del género Pinus also determined that root res- ance among the compartments ACKNOWLEDGEMENTS nativas del Valle de México. Thesis. Colegio de Post- piration rates remained the of the seedlings. Wood accu- graduados. Mexico. 109 pp. same in ozone-exposed seed- mulation in shoots also gener- The authors thank Dave Hérnandez-Tejeda T, Cox RM, lings as in control plants. ated a significant (p<0.05) in- Perry, and Colegio de Post- graduados for allowing to use Malcolm J, de la Isla BML, Their finding further indicated crease in the wood/foliage ra- Vargas HJ, Velázquez MA, that the reduced root biomass tio (Table III) with increasing the facilities needed for both Alvarado RD (2001) Impacto in damaged seedlings is due damage. This imbalance may field and laboratory studies. del ozono sobre el polen de to a decreased carbon alloca- be especially important during Pinus hartwegii Lindl. Rev. 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