SciELO - Scientific Electronic Library Online

 
vol.95 número1Efecto de borde sobre la estructura poblacional y el éxito reproductivo de dos especies de BurseraDeterminantes climáticos del tamaño de las bellotas y el porcentaje de germinación de Quercus rugosa (Fagaceae) a lo largo de un gradiente latitudinal en México índice de autoresíndice de materiabúsqueda de artículos
Home Pagelista alfabética de revistas  

Servicios Personalizados

Revista

Articulo

Indicadores

Links relacionados

  • No hay artículos similaresSimilares en SciELO

Compartir


Botanical Sciences

versión On-line ISSN 2007-4476versión impresa ISSN 2007-4298

Bot. sci vol.95 no.1 México ene./mar. 2017

https://doi.org/10.17129/botsci.626 

Ecology

Reproductive phenology of Sambucus nigra subsp. canadensis in the Abies religiosa temperate forest of the Magdalena river basin, Mexico City

Fenología reproductiva de Sambucus nigra subsp. canadensis en el bosque templado de Abies religiosa de la cuenca del río Magdalena D.F. México

Leticia Bonilla-Valencia1 

Silvia Castillo-Argüero1  * 

Yuriana Martínez-Orea1 

1 Departamento de Ecología y Recursos Naturales. Facultad de Ciencias. Universidad Nacional Autónoma de México.


Abstract:

Background.

Reproductive phenology studies in temperate forests of Mexico are scarce and none of them takes into account micro-environmental factors. As an example, there are no studies of the reproductive dynamics of Sambucus nigra subsp. canadensis, the elderberry.

Questions.

How do environmental factors, at general and micro-scales are related to the production of flowers and fruits of Sambucus nigra subsp. canadensis?

Study species.

Sambucus nigra subsp. canadensis is distributed in Abies religiosa (fir) forests of Mexico and it is associated to areas of anthropogenic disturbance.

Study site and dates.

Temperate forest in the Magdalena river basin, April 2012 to May 2013.

Methods.

The percentages of flowers and fruits of 103 individuals were registered and precipitation, temperature, light and soil chemical properties were characterized as well. To find out the relation between reproductive phenology and the environmental factors we carried out Spearman´s correlations as well as a Canonical Correspondence Analysis for the micro- environmental factors.

Results.

Percentages of flowers and fruits showed a relation with the general factors of precipitation, temperature and light. In the micro-environments with the highest light amounts the percentages of fruits were the highest, while the microenvironments with the highest nitrogen, organic matter concentrations and soil moisture, showed the highest flower percentages.

Conclusions.

We showed that general factors as well as micro-environmental ones have an influence on the proportions of flowers and fruits of the study species in different ways, these knowledges show the reproductive dynamics of this species.

Key words: temperate forest; phenology; flowering; fructification

Resumen:

Antecedentes.

Los estudios de fenología reproductiva en los bosques templados de México son escasos y ninguno toma en cuenta los factores microambientales. Por ejemplo para Sambucus nigra subsp. canadensis el “sauco” no hay estudios de su dinámica reproductiva.

Preguntas.

¿Cómo los factores ambientales generales y microambientales se relacionan con la producción de flores y frutos de Sambucus nigra subsp. canadensis?

Especie de estudio.

Sambucus nigra subsp. canadensis distribuido en los bosques de Abies religiosa (oyamel) de México, es asociado a zonas de disturbio antrópico.

Sitio de estudio y fechas.

Bosque templado de A. religiosa de la Cuenca del río Magdalena en el valle de México de abril de 2012 a mayo de 2013.

Métodos.

Se registró el porcentaje de flores y frutos de 103 individuos y se caracterizaron las condiciones de precipitación, temperatura, luz y propiedades químicas del suelo. Para la relación entre le fenología reproductiva y los factores ambientales se realizaron correlaciones de Spearman y para los factores microambientales un Análisis de Correspondencia Canónica (CCA).

Resultados.

Los porcentajes de flores y frutos se relacionaron con los factores generales de precipitación, temperatura y luz. En los microambientes con mayor cantidad de luz fue mayor el porcentaje de frutos, mientras que en los microambientes con mayor nitrógeno, materia orgánica y humedad del suelo presentaron mayor proporción de flores.

Conclusiones.

Se demostró que los factores generales y microambientales influyen de manera distinta en la proporción de flores y frutos del taxón. Conocimientos que muestran su dinámica reproductiva.

Palabras clave: bosque templado; fenología; floración; fructificación

Reproductive phenology studies the temporal frequency of flowering and fructification stages of plant life cycle and their relationship with environmental factors (Rathcke & Lacey 1985, Borchert 1994). These reproductive structures are involved in the formation and maturation of seeds, as well as in their dispersal, and they determine the regeneration of individuals in a community. Therefore the reproductive phenology represents the first approximation to understand the dynamics of the reproductive success of plants (Rathcke & Lacey 1985, Donohue 2009).

Abiotic factors are signals that trigger the development of the reproductive structures (Rathcke & Lacey 1985, Borchert 1994, Valdez-Hernández et al. 2010). For example in temperate forests of Mexico it has been found that the rainy season matches with the beginning of flower and fruit production in tree species (Cornejo-Tenorio & Ibarra-Manríquez 2007, Cortés-Flores et al. 2013). However environmental factors such as temperature, humidity, light amount and its quality as well as soil chemical properties change in a single area. These variations generate micro-environments, which can be defined as local modifications of weather and they are the result of the spatial differences in altitude, slope and orientation in a site (Chen et al. 1995).

In a similar way these environmental variations give result to different flowering and fructification patterns of individuals of the same species growing in the same area (Donohue 2009, Anderson et al. 2012). This plasticity is an attribute of plants that allows them to ensure survival and reproduction, mainly in heterogeneous and changing ecosystems (Sultan 2000, Hernández-Verdugo et al. 2015).

The study of reproductive phenology at a micro-environmental scale, allows knowing which are the abiotic factors that favor reproductive success in plants. In this sense, current studies on reproductive phenology in temperate forests of Mexico are scarce and none of them considers the space and time heterogeneity generated by micro-environments (Cortés-Flores et al. 2013).

For example in Mexico, an important species that lacks ecological studies is Sambucus nigra L. subsp. canadensis, although it is considered a characteristic species of Abies religiosa temperate forests located between 2,500 and 2,800 m a.s.l. (Arreguín-Sánchez 2001, Applequist 2013). Besides its biological importance, the study of this species is interesting because of the ecological differences that sets it apart from its sister subspecies S. nigra subsp. nigra, which has been cataloged as one of the main invasive weed species of Europe (Atkinson & Atkinson, 2002; Kabuce & Priede 2006). In contrast, S. nigra subsp. canadensis is considered as a natural element of temperate forests in America (Arreguín-Sánchez 2001, Applequist 2013, Hanan-Alipi et al. 2009).

In the Abies religiosa forest, also named fir forest, in the Magdalena river basin (MRB), Mexico City, individuals of Sambucus nigra subsp. canadensis are distributed in an aggregate pattern in open canopy areas with signs of anthropogenic disturbance (Santibáñez-Andrade 2009). This study evaluates the relation of its reproductive phenology with the environmental factors of precipitation, temperature, amount of light and chemical characteristics of the soil, with the objective to know how each one of them influences its reproductive dynamics.

Materials and methods

Study site. The Abies religiosa forest in the Magdalena river basin (MRB) is in the SW of the valley of Mexico between 2,900 and 3,650 m a.s.l. located at 19° 13’ 53’’, 19° 18’ 12’’ N y 99° 14’ 50’’, 99° 20’ 30’ O, covering an extension of 3,100 ha (Figure 1A and B). It is a highly heterogeneous and species rich site, that belongs to the remaining vegetation and soil conservation area of Mexico City (Santibáñez-Andrade et al. 2015).

Figure 1 Study area A) Mexico City location, B) Magdalena river basin location (MRB) in Mexico City and C) Landscape unit number 8 in the Abies religiosa forest of the MRB (Map of Mexico and Mexico City modified from Galeana-Pizaña et al. 2013). 

According to Köppen´s classification, it has a temperate subhumid weather C(w2)(w)b(i’), it has a minimum temperature of 14 ºC, a maximum of 20 ºC and a mean one of 18 ºC, an annual precipitation of 950-1,300 mm (Dobler-Morales 2010) (Figure 2). The forest canopy is dominated by Abies religiosa, Sambucus nigra subsp. canadensis and Salix paradoxa, while other genders such as Senecio, Salvia and Ageratina are found in the understorey (Santibáñez-Andrade et al. 2015).

Figure 2 Climograph from the weather stations of Desviación Alta al Pedregal (1967-2000) and Monte Alegre (1967-1987) (modified from Delgadillo-Durán 2011). 

Species description. Sambucus nigra subsp. canadensis (Adoxaceae), known as the elderberry, is a shrub or tree that grows up to 15 m height. It has corymbs inflorescences, with small, less than1 cm diameter bisexual, white flowers, with five petals. The fruit when mature is a glossy dark purple to black round drupe, of 3-8 mm diameter that contains 3-5 seeds (Figure 3) (Arreguín-Sánchez 2001, Atkinson & Atkinson 2002). Flowers are polinized by bees, beetles and flies, while fruits are mainly bird dispersed (Debussche & Isenmann 1994).

Figure 3 Reproductive structures of Sambucus nigra subsp. canadensis A) White inflorescences, B) Drupes (fruits) and C) Adult. (Drupes modified from Kabuce and Priede, 2006). 

The Abies religiosa forest of the MRB is integrated by 11 landscape units based on their topographic and vegetation features (Santibáñez-Andrade et al. 2015). This study was carried out in the landscape unit number eight (Figure 1C), since it has an important abundance of Sambucus nigra subsp. canadensis in areas of anthropogenic disturbance (Santibáñez-Andrade 2009). In this unit seven plots of 25 × 25 m were selected, following a simple-random method, they were established through their location on (x, y) coordinates, leaving at least 50 m of distance between them, having at least 15 individuals per plot. In each plot we marked all the elderberry individuals that were higher than 3 m height and with reproductive structures, having a total of 103 individuals.

We registered the percentages of young and mature flowers and fruits monthly and during a year (April 2012 to May 2013). We considered the open flowers as mature ones and flower buds as the young ones. Purple fruits were considered as mature ones and those green as young ones. To determine the amounts of young and mature flowers and fruits per individual we used the percentage scale proposed by Fournier and Charpantier (1975) and modified by Carabias-Lillo and Guevara-Sada (1985), in which, in a scale of one to five the percentage of flowers and fruits is estimated with respect to the total of branches (Table 1).

Table 1 Scale proposed by Fournier and Charpantier (1974) and modified by Carabias-Lillo and Guevara-Sada (1995). 

Rank Percentages of reproductive structures
0 Absence of the structure
1 Presence of the structure, in an interval of 1-10%
2 Presence of the structure in an interval of 11-25%
3 Presence of the structure in an interval of 26-50%
4 Presence of the structure in an interval of 51-75%
5 Presence of the structure in an interval of 76-100%

With the aim of knowing the synchrony in time of flowering and fructification between the individuals of Sambucus nigra subsp. canadensis, we calculated the index proposed by Augspurger (1983) through the following equation:

Xi=(1/n1)(1/fi)j=1nej1 [1]

Where: Xi is the individual synchrony index, n is the number of individuals in the population, fi is the number of days in which the individual i has a phenological event and e.g. is the number of days in which both individuals i and j have a phenological event in common.

With the individual synchrony index, we obtained the population synchrony index (Z) with the equation proposed by Augspurger (1983):

Z=(1/n)j=1nXi [2]

Where: Z represents the population synchrony index, n is the number of individuals in the population and Xi is the synchrony index per individual obtained with equation [1]. When Z equals one, individuals in the population show complete synchrony.

From April 2012 to May 2013 the means of monthly precipitation were consulted in the weather station of Monte Alegre D.F (SMN 2013). In order to register the environmental temperatures during the study year continuously, in each plot a HOBO data logger (HOBO Onset Corporation USA) was installed at the soil surface. With the aim to characterize the light conditions in the plots, every two months at 8 o´clock in the morning, we took three hemispheric photographs (Nikon digital camera Nikon D80 with a “fisheye” lens EX SIGMA 4.5 2:28 DCHSM), for all of them, the superior part of the lens facing north. They were analyzed with the Gap Light Analyzer GLA, 2.0 (Frazer et al. 2000) software, to determine the canopy gap fraction (CGF) and the global site factor (GSF), that is defined as the percentage of light transmitted (in moles), and it was calculated according to Canham et al. (1990) with the following equation:

GSF=(FSDFSI)/2 [3]

Where: GSF is the global site factor, FSD is the percentage of direct light and FSI is the percentage of diffuse light.

In both seasons of the year, dry and rainy, in each plot five soil samples of 250 g of the first 10 cm and without litter were taken. Four samples corresponded to the corners of the plot and one more to the center of it. These were combined per plot and were sent to the soil fertility laboratory in the Colegio de Postgraduados campus Montecillo, for their chemical analysis. Analyzed variables were pH, through the relation of soil and water 1:2, electric conductivity in water (E.C.), with the relation 1:5 and an electric conductivity bonding, percentage of organic matter (O.M.), through a humid digestion with Walkley-Black determination, and the availability of inorganic phosphorus (P) concentration was obtained through the extraction of NaHCO3 0.5 M (pH 8.5) and with colorimetric determination. The percentage of nitrogen (N) was determined as well, with a moist digestion with a mixture of sulfuric acid with Kjeldahl distillation through a steam stripping and a sulfuric acid 0.05 N tritation. Potassium (K) concentration was determined as well, with a pH 7 NH4OAc extraction through flame photometry. In order to know the moisture content of the soil in the study plots, every two months soil samples were weighed and oven dried at 100 °C, moisture content percentage was calculated through the Reynold’s (1970) equation:

H%=((WemoWedr)/Wdr)×100 [4]

Where: H% is the soil moisture, Wemo is the weight of the moist soil, Wedr is the weight of the dry soil.

Analysis. The evaluated variables did not show a normal distribution when tested with Shapiro-Wilk, therefore the correlations between the percentages of flowers and mature fruits with the environmental variables were calculated through the Spearman´s test with the STATISTICA 8 software (Stat Soft, Inc. 2007). With the objective to know the relation between the environmental factors of the dry and the rainy seasons in the seven plots and the young flowers and fruits of the individuals, we carried out a Canonical Correspondence Analysis (CCA) with the software PC-ORD version 5.10 (McCune & Mefford 2006). The evaluated micro-environmental characteristics in this study were analyzed with the ANOVA and Tukey (P < 0.05) multiple comparisons tests. The micro-environmental differences in electric conductivity, organic matter and potassium concentration that did not show a normal distribution, were analyzed with the Kruskal-Wallis and Student-Newman-Keuls (P < 0.05) multiple comparisons tests non parametric statistic test with STATISTICA 8 (Stat Soft, Inc. 2007) (P < 0.05) software.

Results

Relation between the reproductive phenology and the environmental factors. From March to October Sambucus nigra subsp. canadensis showed reproductive structures (Figure 4). The main flowering season was from March to June, and a second, less intense flowering season was detected in September (Figura 4). Most individuals (66 %) showed the highest percentage of flowers (26.67 %) in May. Fruits were observed from May to October and the maximum percentage of fruits was reached in July (30 %), however an important increase of individuals with fruits (47 %) was registered in August (Figure 4). In the population level, a low synchrony of the reproductive phases was observed: the synchrony index value for flowering was 0.47 and 0.24 for fructification.

Figure 4 Reproductive phenology pattern of Sambucus nigra subsp. canadensis; monthly percentages of individuals with flowers and fruits (primary axis). Monthly percentages of flowers and fruits (secondary axis). 

According to the relation between reproductive phenology and the environmental factors, the percentages of flowering were correlated in a significant and positive way with the canopy gap fraction (% CGF) and in a negative way with the soil moisture content (P < 0.05). Percentages of fruits were correlated in a significant and positive way with the precipitation and temperature (P < 0.05) (Table 2).

Table 2 Spearman’s rank correlation coefficient values (rs) between the percentages of flowers and fruits and the abiotic factors (P < 0.05) (*significant differences). 

Flowers (%) Fruits (%)
Precipitation (mm) 0.07 *0.89
Temperature (º C) 0.45 *0.82
Light (% GSF) 0.43 -0.16
Canopy gap (% CGF) 0.67* 0.15
Soil moisture content (%) -0.63* 0.06

Micro-environmental groups. The Canonical Correspondence Analysis (CCA) between reproductive phenology and the environmental factors, identified three micro-environmental groups, and their explained variance was 50.9 % for axis 1 and 28.3 % for the second variation axis (Table 3). The results of the Monte Carlo permutations test indicated that the ordination provides a significant representation of the percentages of flowers and fruits and the registered environmental variables (P < 0.05). In group one (plots five and two) the percentages of young fruits in the dry and rainy seasons, as well as the mature fruits percentages of the dry season, were related in a positive way with the amount of light (GSF) (Figure 5). In micro-environment two (plots one and three) the increase in mature flowers during the dry and rainy seasons, was related in a positive way with high values of organic matter (O.M.), nitrogen (N), soil moisture and phosphorus (P), this last was the one with the smallest relation (Figure 5). Micro-environment three (plots seven and four) did not show any direct association between reproductive phenology and the micro-environmental factors (Figure 5).

Table 3 Statistical summary for Canonical Correspondence Analysis (CCA). 

Axis 1 Axis 2
Eigenvalues 0.071 0.039
Variance explainded (%) 50.9 28.3
Variance comulative (%) 50.9 79.2
Pearson Correlatión 1.00 1.00

Figure 5 Canonical Correspondence Analysis (CCA) of the reproductive phenology of Sambucus nigra subsp. canadensis and the abiotic factors in the dry and rainy seasons; par = plot and number, fl = flowers, fr = fruits, yo = young, ma = mature, dr= dry season, ra = rainy season, Moistra = soil moisture content in the rainy season , MO = organic matter, N = nitrogen, P = phosphorus, GSFra = global site factor in the rainy season and GSFdr = global site factor in the dry season. 

Reproductive phenology of the micro-environmental groups. The reproductive phenology pattern was different between the three micro-environments (Figure 6). However, no significant differences were found for the percentages of flower and fruit numbers during the year (F3,284 = 0.24, P = 0.76 and F3.284 = 2.00, P = 0.15 respectively).

Figure 6 Monthly percentages of flowers and fruits in the three micro-environmental groups and hemispheric photographs of each micro-environment; A) Group one, B) Group two and C) Group three. 

The individuals of the micro-environmental group one showed the highest percentage of fruits in July (47 %) (Figure 6A) and the highest synchrony index value (Z = 0.23, Table 4). In the case of the individuals in group two, both the percentages of flowers and fruits reached values close to 30 % (Figure 6B), in this micro-environment the highest synchrony index value for flowering was observed (Z = 0.22), as well as the highest percentage of soil moisture content (60 ± 34.26), M.O. amount (20 ± 0.41) and of N (0.66 ± 0.01). Analysis of variance for the three micro-environmental groups showed that the amounts of O.M. and N are significantly different between them (K13.91, P < 0.001 and F1,215 = 15.4, P < 0.001 respectively) (Table 4). Finally, the individuals of micro-environment three stand out since they showed the lowest percentages of reproductive structures (< 21 %) (Figure 6C).

Table 4 Comparison of the micro-environmental characteristics and the synchrony index values for flowers and fruits in the three micro-environmental groups (*, ** significant differences P < 0.05). 

Group 1 Group 2 Group 3
Canopy gap (% CGF) 17.39 ± 5.92 15.72 ± 5.55 15.91 ± 5.31
Light (% GSF) 23.34 ± 7.09 21.85 ± 8.33 24.82 ± 6.53
Organic matter (O.M) (% W-B) *16.20 ± 1.76 *20.50 ± 0.41 **19.60 ± 0.97
Nitrogen (N) ( % Kjeldahl) *0.59 ± 0.01 **0.66 ± 0.01 **0.66 ± 0.042
Phosphorus (P) (mg/Kg) 4 ± 1.60 6 ± 2.47 6 ± 2.91
Potassium (K)(meq/100g) 0.8 ± 0.19 0.7 ± 0.06 0.8 ± 0.24
pH (1:2 H2O) 5.7 ± 0.16 5.5 ± 0.19 5.7 ± 0.33
Electric conductivity (E.C) (dS/m 1:5 H2O) 0.05 ± 0.003 0.05 ± 0.004 0.05 ± 0.003
Moisture content (%) 46.76 ± 19.21 60.42 ± 34.26 55.35 ± 25.98
Flowers synchrony index (Z) 0.13 0.22 0.12
Fruits synchrony index (Z) 0.23 0.08 0.07

Discussion

Reproductive phenology of tree species in temperate forests of Mexico is directly related to the precipitation season (Cornejo-Tenorio & Ibarra-Manríquez 2007; Cortés-Flores et al. 2013). This is also the case of the studied species: the general pattern of the reproductive phenology of Sambucus nigra subsp. canadensis showed a relation with the rainy season, in particular in terms of the fructification pattern. Ramírez-García & Nepamuceno-Martínez (1986) and Cornejo-Tenorio & Ibarra-Manríquez (2007) suggest that most of fleshy fruits are produced during the highest precipitation season, since big quantities of water are needed for their maturation. This coincides with the findings of our study, since the percentages of S. nigra subsp. canadensis fruits were positively correlated to precipitation.

Water availability for plants does not only depend on the changes in precipitation, but also on soil moisture content. This is why phenology studies besides taking into account the precipitation values, they should also search about the role of soil moisture content (Borchert 1994). In the case of Sambucus nigra subsp. canadensis the negative relation between the soil moisture and flower percentages, suggests that low contents of soil moisture favor the development of flowers, result that has also been reported for other tree species of Mexican temperate forests (Cornejo-Tenorio & Ibarra-Manríquez 2007, Cortés-Flores et al. 2013). In this sense several authors such as Borchert (1994) and Seghieri et al. (2009), have suggested that the apparent paradox between water stress conditions and the increase of flowers, is due to the fact that before the beginning of their production, there is a considerable loss of leaves that avoids the loss of water by evapotranspiration, this explanation coincides with our observations in the field. On the other hand, dry season flowering can have an adaptive meaning, since the most intense activity of pollinators has been registered for this season and it is also when there usually is an important decrease of insect pests (Wright & van Schaik 1994, Bolmgren et al. 2003, Kilkenny & Galloway 2008).

Plant reproductive phenology patterns are also modified by changes in temperature. A clear example of this is confirmed by the temperate tree species, in which the proportion of fruits rises up above the mean, during the season of the highest temperatures (Wright & van Schaik 1994, Kramer et al. 2000). In this study the relation between fruit phenology of Sambucus nigra subsp. canadensis and the temperature showed a significant and positive relation. About this Atkinson & Atkinson (2002) have reported that S. nigra subsp. nigra increases the percentage of its fruits in sites with the highest temperatures.

Anther factor that controls plant phenology is light. The maximum flowering periods of temperate forest understorey species have been registered during the season of most light availability and least cloudiness, which corresponds to the beginning of spring, before the increases in canopy cover (Wright & van Schaik 1994, Cornejo-Tenorio & Ibarra-Manríquez 2007). This argument is supported on the results of this research, since there is a positive relation between the canopy openness and the amount of light with the flower production of Sambucus nigra subsp. canadensis.

It has been proposed that the micro-environmental differences in light are conducive to variability in the fructification times between the individuals that grow up in a single area (Williams-Linera 2003). For example, in Sambucus nigra subsp. nigra and Sambucus racemosa, it has been reported that their establishment and fruit production increases in sites with the highest light availability (Atkinson & Atkinson 2002, Abe et al. 2008, Schaefer & Braun 2009). These results coincide with what we found in this study, since in micro-environment one, which showed the highest canopy openness as well as light amount, the individuals of S. nigra subsp. canadensis showed the highest fruit percentages.

Micro-environmental differences in soil chemical properties can influence the reproductive phenology of plants (Valdez-Hernández et al. 2010). The relation between reproductive phenology and chemical soil characteristics has been little studied. However, an increase in flower percentages in soils with highest nitrogen and humidity has been reported (Galen et al. 1999, Zhang et al. 2013). In this study the highest percentages of Sambucus nigra subsp. canadensis flowers were found in the most humid sites, with highest soil organic matter. The close relation between these characteristics, could be due to the fact that in the decomposition process organic matter is produced and the release of nitrogen by microorganisms is favored, this interaction also promotes the formation of organo-mineral complexes (Liebig et al. 2004).

Although micro-environmental conditions influence the flowering and fructification patterns, the adaptive response is different between the individuals in a population, and it can be independent of environmental factors (Danuso et al. 2012, Post et al. 2001). In this work, the study site includes micro-environmental conditions that did not show a direct relation with the reproductive phenology for all the individuals. For example reproductive phenology of the individuals in group three, did not show any relation with the evaluated micro-environmental variables. Other random factors, or the genetic constitution of individuals, plant diseases, pollination interactions, dispersal and predation can influence the variability of reproductive patterns (van Schaik et al. 1993, Cuevas-García et al. 2013, Alvarado et al. 2014). Likewise, the temporal variability between years can display the relation between environmental factors and the production of reproductive structures at a finer scale (Sherry et al. 2007). The results of our study only consider the environmental variability of one year.

On the other side, in ecosystems that are under continuous anthropic disturbances, micro-environmental changes occur rapidly and they can change plant reproductive phenology (Post et al. 2001, Wolkovich & Cleland, 2010). With respect to this Post et al. (2001) point out those reproductive patterns synchrony tends to be small in conditions of frequent disturbances. Wider distribution and higher abundances of Sambucus nigra subsp. canadensis have been found in perturbed areas (Santibáñez-Andrade 2009). This coincides with our results, because small values of synchrony were registered in the three micro-environments. Since patterns of flowering and fructification are a reflex of the opportunities for pollination and dispersal (Augspurger 1983, Pires et al. 2014) and taking into account the predictions proposed by Post et al. (2001), for species under anthropic disturbances, the small values of synchrony indexes of S. nigra subsp. canadensis suggest that pollinators and dispersers are available during most of the year and they do not present a marked seasonality.

This study is the first approach to the reproductive ecology of Sambucus nigra subsp. canadensis in Mexico. The importance of this research is based in knowing the reproductive dynamics of a disturbance indicator species that shows high importance values in these areas (Santibáñez-Andrade 2009). According to our results, S. nigra subsp. canadensis shows different flowering and fructification patterns in the evaluated micro-environments. The micro-environment with the highest values of nitrogen, organic matter and soil moisture content was the one with the highest percentages of flowers, and the micro-environment with the highest amounts of light was the one that showed a high proportion of fruits. The relation between a higher fruit proportion and high amounts of light has already been reported for its sister subspecies, S. nigra subsp. nigra, which is considered as one of the main invasive and weed species of Europe (Atkinson & Atkinson 2002, Kabuce & Priede 2006). For Atkinson & Atkinson (2002) this close relation is one of the main characteristics that promotes its colonization in temperate forests under anthropic disturbances, since the generation of forest gaps is one of the main perturbations promoted by deforestation.

The data obtained in this work do not exclude the possibility that Sambucus nigra subsp. canadensis can turn into a weed or invasive species, if the ecological dynamics of this community is perturbed by anthropic disturbances. However, in order to determine a species as invasive and/or weed, it is necessary to know its biogeographic origin, its distribution area and to evaluate the dynamics of its reproductive success in the long term, through its reproductive phenology, germination and survival (Richardson et al. 2000, Wolkovich & Cleland 2010, Danuso et al. 2012). In the case of S. nigra subsp. canadensis little is known about its ecology. Therefore it is necessary to continue the study of its reproductive phenology in order to determine how micro-environmental differences can influence other characteristics of its life history, such as germination and survival, as well as to understand the ecological role of this species in Mexican temperate forests.

Acknowledgments

To Marco Romero Romero for his support in figure editing, to projects PAPIIT IN-216014 DGAPA UNAM and PAPIME PE-204413. The authors thank the anonymous reviewers that helped us improve this document.

Literatura Cited

Abe S, Motai H, Tanaka H, Shibata M, Kominam Y, Nakashizuka T. 2008. Population maintenance of the short-lived shrub Sambucus in a deciduous forest. Ecology 89:1155-1167. DOI:10.1002/ecy.1552. [ Links ]

Alvarado ST, Buisson E, Rabarison H, Rajeriarison C, Birkinshaw C, Lowry II PP, Morellato LPC. 2014. Fire and the reproductive phenology of endangered Madagascar Sclerophyllous tapia woodlands. South African Journal of Botany 94:79-87. DOI:doi.org/10.1016/j.sajb.2016.09.008. [ Links ]

Anderson JT, Inouye DW, McKinney AM, Colautti RI Mitchell-Olds T. 2012. Phenotypic plasticity and adaptive evolution contribute to advancing flowering phenology in response to climate change. Proceedings of the Royal Society B 282:3843-3852. DOI: 10.1098/rspb.2012.105. [ Links ]

Applequist WL. 2013. A brief review of recent controversies in the taxonomy and nomenclature of Sambucus nigra sensu lato. Acta Horticulturae 1061:25-33. [ Links ]

Arreguín-Sánchez ML. 2001. Sambucus nigra L. In: Calderón de Rzedowski G, Rzedowski J, eds. Flora Fanerogámica del Valle de México. Xalapa: Instituto de Ecología, A.C. y Comisión Nacional para el Conocimiento y Uso de la Biodiversidad, 738. ISBN 970-9000-17-9. [ Links ]

Atkinson MD, Atkinson E. 2002. Sambucus nigra L. Journal of Ecology 90:895-923. DOI: 10.1111/1365-2745.12675. [ Links ]

Augspurger CK. 1983. Phenology, flowering synchrony and fruit set of six neotropical shrubs. Biotropica 15: 257-267. DOI: 10.1111/btp.12370. [ Links ]

Bolmgren K, Eriksson O, Linder HP. 2003. Contrasting flowering phenology and species richness in abiotically and biotically pollinated angiosperms. Evolution 57: 2001-2011. DOI:10.1111/evo.13088. [ Links ]

Borchert R. 1994. Soil and stem water storage determine phenology and distribution of tropical dry forest trees. Ecology 75:1437-1449. DOI:10.1002/ecy.1552. [ Links ]

Canham CD, Denslow JS, Platt WJ, Runkle JR, Spies TA, White PS. 1990. Light regimes beneath closed canopies and tree-fall gaps in temperate and tropical forests. Canadian Journal of Forest Research 20:620-631. DOI:10.1139/x90-013. [ Links ]

Carabias-Lillo J, Guevara-Sada S. 1985. Fenología de una selva tropical húmeda y en una comunidad derivada: Los Tuxtlas, Veracruz. In: Gómez-Pompa A, Del Amo-R S, eds. Investigaciones sobre la Regeneración de Selvas Altas en Veracruz, México. Vol. II Xalapa: Instituto Nacional de Investigaciones sobre Recursos Bióticos, 27-66. [ Links ]

Chen J, Franklin JF, Spies TA. 1995. Growing-season microclimate gradients from clear-cut edges into old-growth Douglas-fir forests. Ecological Applications 5:74-86. DOI: 10.2307/1942053. [ Links ]

Cornejo-Tenorio G, Ibarra-Manríquez G. 2007. Plant reproductive phenology in a temperate forest of the Monarch Butterfly Biosphere Reserve, Mexico. Interciencia 32:445-452. DOI: 10.6084/m9.figshare.1116224. [ Links ]

Cortés-Flores J, Andresen G, Cornejo-Tenorio G, Ibarra-Manríquez G. 2013. Fruiting phenology of seed dispersal syndromes in a Mexican neotropical temperate forest. Forest Ecology and Management 289:445-454. DOI:org/10.1016/j.foreco.2012.10.038. [ Links ]

Cuevas-García E, Alcalá-Guerra A, Baños-Bravo YE, Flores-Palacios A. 2013. Biología reproductiva y robo de néctar en Salvia gesneriflora (Lamiaceae) y sus consecuencias en el éxito reproductivo. Botanical Sciences 91:357-362. DOI:dx.doi.org/10.17129/botsci.237. [ Links ]

Danuso F, Zanin G, Sartorato I. 2012. A modelling approach for evaluating phenology and adaptation of two congeneric weeds (Bidens frondosa and Bidens tripartita). Ecological Modelling 243:33-41. DOI:org/10.1016/j.ecolmodel.2012.06.009. [ Links ]

Debussche M, Isenmann P. 1994. Bird-dispersed seed rain and seedling establishment in patchy mediterranean vegetation. Oikos 69:414-426. DOI:10.2307/3545854. [ Links ]

Delgadillo-Durán E. 2011. Productividad primaria neta de los bosques templados de la cuenca del río Magdalena. MSc. thesis, Facultad de Ciencias, Universidad Nacional Autónoma de México. [ Links ]

Dobler-Morales E. 2010. Caracterización del clima y su relación con la distribución de la vegetación en el suroeste del D.F. México. BSc.Thesis, Facultad de Ciencias, Universidad Nacional Autónoma de México. [ Links ]

Donohue K. 2009. Completing the cycle: maternal effects as the missing link in plant life histories. Philosophical Transactions of the Royal Society B 364:1059-1074. DOI:10.1098/rstb.2008.0291. [ Links ]

Fournier-O LA and Charpantier C. 1975. El tamaño de la muestra y la frecuencia de las observaciones en el estudio de las características fenológicas de los árboles tropicales. Turrialba 25:44-48. [ Links ]

Frazer GW, Canham CD, Lertzman KP. 1999. Gap Light Analyzer (GLA), version 2.0: Imaging software to extract canopy structure and gap light transmission indices from true-colour fisheye photographs, users manual and program documentation. Simon Fraser University/Institute of Ecosystem Studies, Millbrook, New York. [ Links ]

Galeana-Pizaña JM, Ordóñez-Díaz JA B, Corona-Romero N. 2013. Estimación de contenido de carbono en la cuenca del río Magdalena, México. Madera y Bosques 19:53-69. ISSN 1405-0471. [ Links ]

Galen C, Sherry RA, Carroll AB. 1999. Are flowers physiological sinks or faucets? Costs and correlates of water use by flowers of Polemonium viscosum. Oecologia 118:461-470. DOI: 10.1007/s004420050749. [ Links ]

Hanan-Alipi A, Mondragón-Pichardo J and Vibrans H. 2009. Sambucus nigra var. canadensis. In: Vibrans H . (ed.) Malezas de Mexico. <http://www.conabio.gob.mx/malezasdemexico/caprifoliaceae/sambucus-nigra/fichas/pagina1.htm > (accessed January 12, 2015). [ Links ]

Hernández-Verdugo S, González-Sánchez RA, Porras F, Parra-Terraza S, Valdez-Ortiz A, Pacheco-Olvera A, López-España G. 2015. Plasticidad fenotípica de poblaciones de chile silvestre (Capsicum annuum var. glabriusculum) en respuesta a disponibilidad de luz. Botanical Sciences 92:231-240. DOI:dx.doi.org/10.17129/botsci.237. [ Links ]

Kabuce N, Priede N. 2006. Invasive alien species fact sheet Sambucus nigra. From Online Database of the European Network on Invasive Alien Species - NOBANIS. < https://www.nobanis.org/globalassets/speciesinfo/s/sambucus-nigra/sambucus-nigra.pdf > (accessed December 19, 2015). [ Links ]

Kilkenny FF, Galloway LF. 2008. Reproductive success in varying light environments: direct and indirect effects of light on plants and pollinators. Oecologia 155:247-255. DOI: 10.1007/s004420050749. [ Links ]

Kramer, K, Leinonen I, Loustau D. 2000. The importance of phenology for the evaluation of impact of climate change on growth of boreal, temperate and Mediterranean forest ecosystems: an overview. International Jornal of Biometeorology 44:67-75. DOI: 10.1007/s004840000066. [ Links ]

Liebig MA, Tanaka DP, Wienhold BJ. 2004. Tillage and cropping effects on soil quality indicators in the northern Great Plains. Soil and Tillage Research 78:131-141. DOI:dx.doi.org/10.1016/j.still.2016.09.013. [ Links ]

McCune B, Mefford MJ. 2006. PC-ORD. Multivariate analysis of ecological data. Version 5.10. MjM Software. [ Links ]

Pires JPA, Da Silva AG, Freitas L. 2014. Plant size, flowering synchrony and edge effects: What, how and where they affect the reproductive success of a neotropical tree species. Austral Ecology 39:328-336. DOI:10.1002/ecy.1552. [ Links ]

Post E, Levin SA, Iwasa Y, Stenseth NC. 2001. Reproductive asynchrony increases with environmental disturbance. Evolution 55:830-834. DOI:10.1111/evo.13088. [ Links ]

Ramírez-García JA, Nepamuceno-Martínez F. 1986. Fenología de tres especies de coníferas de la región de Los “Altos de Chipas”. Ciencia Forestal 60:21-50. ISSN:2448-6671. [ Links ]

Rathcke B, Lacey EP. 1985. Phenological patterns of terrestrial plants. Annual Review of Ecology and Systematics 16:179-214. DOI:10.1146/annurev.es.16.110185.001143. [ Links ]

Reynolds SG. 1970. The gravimetric method of soil moisture determination, Part I: A study of equipment and methodological problems. Journal of Hydrology 11:258-273. DOI:dx.doi.org/10.1016. [ Links ]

Richardson DM, Pyšek P, Rejmánek M, Barbour MG, Panetta FD, West CJ. 2000. Naturalization and invasion of alien plants: concepts and definitions. Diversity and Distributions 6:93-107. DOI:10.1046/j.1472-4642.2000.00083.x. [ Links ]

Santibáñez-Andrade G. 2009. Composición y estructura del bosque de Abies religiosa en función de la heterogeneidad ambiental y determinación de su grado de conservación en la cuenca del río Magdalena, México., D.F. MSc. thesis, Facultad de Ciencias, Universidad Nacional Autónoma de México. [ Links ]

Santibáñez-Andrade G, Castillo-Argüero S, Zavala-Hurtado JA, Lindig Cisneros R, Vega-Peña EV. 2015. Structural equation modeling as a tool to develop conservation strategies using environmental indicators: The case of the forests of the Magdalena river basin in Mexico City. Ecological Indicators 54:124-136. DOI:dx.doi.org/10.1016/j.ecolind.2015.02.022. [ Links ]

Schaefer HM, Braun J. 2009. Reliable cues and signals of fruit quality are contingent on the habitat in black elder (Sambucus nigra). Ecology 90:1564-1573. DOI:10.1002/ecy.1552. [ Links ]

Seghieri J, Vescovo A, Padel K, Soubie R, Arjounin M, Boulain N, De Rosnay P, Galle S, Gosset M, Mouctar AH, Peugeot C, Timouk F. 2009. Relationships between climate, soil moisture and phenology of the woody cover in two sites located along the West African latitudinal gradient. Journal of Hydrology 375: 78-89. DOI:dx.doi.org/10.1016. [ Links ]

Sherry RA, Zhou X, Gu S, Arnone JA, Schimel DS, Verburg PS, Luo Y, Wallace LL. 2007. Divergence of reproductive phenology under climate warming. Proceedings of the National Academy of Sciences of the United States of America 104:198-202. DOI:10.1073/pnas.0605642104. [ Links ]

SMN. 2013. Sistema Meteorológico Nacional México. Comisión Nacional del Agua. <http://www.smn.gob.mx > (accessed October 25, 2013). [ Links ]

Stat Soft, Inc. 2007. STATISTICA (data analysis software system), version 8.0. http://www.Statsoft.com (accessed September 20,2013). [ Links ]

Sultan SE. 2000. Phenotypic plasticity for plant development, function and life history. Trends in Plant Science 5:537-542. DOI:10.1016/S1360-1385(00)01797-0. [ Links ]

Valdez-Hernández M, Andrade JL, Jackson PC, Rebolledo-Vieyra M. 2010. Phenology of five tree species of a tropical dry forest in Yucatán, Mexico: effects of environmental and physiological factors. Plant and Soil 329:155-171. DOI:10.1007/s11104-009-0142-7. [ Links ]

van Schaik CP, Terborgh JW, Wright SJ. 1993. The phenology of tropical forests: adaptive significance and consequences for primary consumers. Annual Review of Ecology and Systematics 24:353-377. DOI:10.1146/annurev.es.24.110193.002033. [ Links ]

Williams-Linera G. 2003. Temporal and spatial phenological variation of understory shrubs in a tropical montane cloud forest. Biotropica 35:28-36. DOI:10.1111/j.1744-7429.2003.tb00259.x. [ Links ]

Wolkovich EM, Cleland EE. 2010. The phenology of plant invasions: a community ecology perspective. Frontiers in Ecology and the Environment 9:287-294. DOI:10.1890/100033. [ Links ]

Wright, SJ, van Schaik CP. 1994. Light and the phenology of tropical trees. The American Naturalist 143:192-199. DOI:10.1086/687963. [ Links ]

Zhang Z, Niu K, Liu X, Jia P, Du G. 2013. Linking flowering and reproductive allocation in response to nitrogen addition in an alpine meadow. Journal of Plant Ecology 7:231-239. DOI:10.1093/jpe/rtt030. [ Links ]

Received: November 10, 2015; Accepted: January 15, 2016

* Corresponding author: Silvia Castillo-Argüero, e-mail: silcas@ciencias.unam.mx

Creative Commons License This is an open-access article distributed under the terms of the Creative Commons Attribution License