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Plant reproductive phenology in a temperate forest of the monarch butterfly biosphere reserve, Mexico/Fenologia reproductiva de las plantas de un bosque templado de la reserva de la biosfera mariposa monarca, Mexico/Fenologia reprodutiva das plantas de um bosque temperado da reserva da Biosfera mariposa monarca, Mexico.

SUMMARY

Monthly flowering and fruiting observations were recorded for the most dominant species (11 annual herbs, 72 perennial herbs, 21 shrubs, and 8 trees) in a temperate forest, during 2004, in the Cerro Altamirano Core Zone of the Monarch Butterfly Biosphere Reserve in central Mexico. Intraspecific synchrony in flowering and fruiting of eight woody species was estimated by monitoring 20 individuals of each. Flowering and fruiting occurred mainly during the rainy season and at the beginning of the dry season (Jul-Dec) and showed a low degree of seasonality. Reproductive activity within growth forms occurred in different periods: 1) annual and perennial herbs flowered principally during the rainy season and at the beginning of the dry season, while their fruiting peaked during the dry season; 2) shrubs produced flowers and fruits throughout the year without peaks in any season; and 3) nearly all trees had flowers and fruits during the dry season. Correlations of the number of flowering species at community level and perennial herbs against rainfall showed a significant positive relationship. However, a negative relationship was found between rainfall and number of fruiting species in shrubs and trees. High reproductive synchrony (>60% of individuals in the same phenological phase) was detected in five tree species. Phenological reproductive patterns in the study area, essentially a temperate high altitude forest in the tropics, were similar to those documented for the seasonal lowland tropical forests, mainly explained by annual rainfall and growth form.

KEYWORDS / Ecosystem Conservation / Flowering Phenology / Fruiting Phenology / Growth Forms / Intraspecific Synchrony /

RESUMEN

Para documentar la fenologia reproductiva de las especies mas importantes (11 hierbas anuales, 72 hierbas perennes, 21 arbustos y 8 arboles) del bosque templado en la zona nucleo Cerro Altamirano, Reserva de la Biosfera Mariposa Monarca, Mexico, se realizaron observaciones mensuales durante 2004. La sincronia intraespecifica de floracion y fructificacion se estimo en ocho especies lenosas por medio de la observacion de 20 individuos por especie. La floracion y fructificacion ocurrio principalmente durante la estacion de lluvias e inicios de la estacion seca (jul-dic), con baja estacionalidad. Las formas de crecimiento mostraron diferencias temporales en su actividad reproductiva: i) las hierbas anuales y perennes florecieron principalmente durante la estacion de Uuvias e inicios de la seca, mientras que la mayoria de especies con frutos fue observada en la estacion seca; ii) los arbustos presentaron flores y frutos a lo largo del ano, sin maximo en alguna epoca particular, y iii) la mayoria de los arboles concentraron su actividad reproductiva en la epoca de menor precipitacion. El numero de especies en floracion a nivel comunitario y de hierbas perennes se correlaciono positivamente con la precipitacion, y el numero de especies arbustivas y arboreas en fructificacion mostro una correlacion negativa con la precipitacion. Se determino una alta sincronia reproductiva (>60% de los individuos en una fase fenologica especifica) en cinco de las especies arboreas. Los patrones fenologicos reproductivos en el area, un bosque templado de elevada altitud en una zona tropical, fueron similares a los documentados para bosques tropicales estacionales de bajas altitudes, y explicados principalmente por la precipitacion total anual y la forma de crecimiento de las especies.

RESUMO

Para documentar a fenologia reprodutiva das especies mais importantes (11 ervas anuais, 72 ervas perenes, 21 arbustos e 8 arvores) do bosque temperado na zona nucleo Cerro Altamirano, Reserva da Biosfera Mariposa Monarca, Mexico, se realizaram observacoes mensais durante 2004. Estimou-se a sincronia intra-especifica na floracao e frutificacao em oito especies lenhosas por meio da observacao de 20 individuos por especie. A floracao e frutificacao ocorreram principalmente durante a estacao de chuvas e inicios da estacao seca (jul-dez), com baixa estacionalidade. As formas de crescimento mostraram diferencas temporais na sua atividade reprodutiva: i) as ervas anuais e perenes floresceram principalmente durante a estacao de chuvas e inicios da seca, enquanto que a maioria de especies com frutos foi observada na estacao seca; ii) os arbustos apresentaram flores e frutos ao longo do ano, sem maximo em alguma epoca em particular, e iii) a maioria das arvores concentraram sua atividade reprodutiva na epoca de menor precipitacao. O numero de especies em floracao a nivel comunitario e de ervas perenes se correlacionou positivamente com a precipitacao, e o numero de especies arbustivas e arboreas em frutificacao mostrou uma correlacao negativa com a precipitacao. Determinou-se uma alta sincronia reprodutiva (>60% dos individuos em uma fase fenologica especifica) em cinco das especies arboreas. Os patroes fenologicos reprodutivos na area, um bosque temperado de elevada altitude em zona tropical, foram similares aos documentados para bosques tropicais estacionais de baixas altitudes, e explicados principalmente pela precipitacao total anual e a forma de crescimento das especies.

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One of the most important aspects of phenology studies is the search of factors that explain the phenological behavior of species. Rainfall, temperature, soil water availability and photoperiod appear to be the main abiotic factors that trigger flowering and fruiting events (van Schaik et al., 1993; Newstrom et al., 1994; Morellato et al., 2000; Borchert et al., 2004). On the other hand, biotic factors such as fruit type, pollination and seed dispersal syndromes are also very important for understanding the flowering and fruiting patterns of plant species (Bawa et al., 1985; Ibarra-Manriquez et al., 1991; Ibarra-Manriquez and Oyama, 1992; van Schaik et al., 1993; Newstrom et al., 1994; Wright and Calderon, 1995; Poulin et al., 1999; Spina et al., 2001; Bolmgren et al., 2003).

An additional recurring focus in plant phenology studies is the comparison of phenological patterns among different growth forms. Several studies have found that herbaceous species produce flowers and fruits during the rainy season, whereas woody species tend to have flowers during the dry season and fruits during the dry or rainy seasons (Frankie et al., 1974; Croat, 1975; Opler et al., 1980; Sarmiento and Monasterio, 1983; Ibarra-Manriquez et al., 1991; Ibarra-Manriquez and Oyama, 1992; Chapman et al., 1999; Batalha and Mantovani, 2000; Ramirez, 2002; Joshi and Janarthanam, 2004). Another important aspect is the intraspecific synchrony in reproductive events. A high degree of synchrony in flowering and fruiting could be advantageous for the plants by increasing the attraction of pollinators and seed dispersers, or the satiation of seed predators (Rathcke and Lacey, 1985; Smith and Bronstein, 1996; Olvera et al., 1997; Kelly and Sork, 2002). In contrast, asynchrony could minimize competition for dispersal agents, propagule predation and pathogen incidence (Rathcke and Lacey, 1985; van Schaik et al., 1993; Poulin et al., 1999).

This work describes for the first time the reproductive plant phenology in one of the core zones of the Monarch Butterfly Biosphere Reserve in central Mexico. This reserve is the winter refuge of the monarch butterfly (Danaus plexippus L.) and is one of the most important protected areas of temperate forest in Mexico, in terms of diversity of vascular plants, area, and its biogeography, which includes a unique combination of northern and southern elements at high elevation within the tropics. To date, phenological studies in Mexico have been conducted mainly on woody species of tropical dry forests and tropical rain-forests (Carabias-Lillo and Guevara, 1985; Bullock and Solis-Magallanes, 1990; Ibarra-Manriquez et al., 1991; Ibarra-Manriquez, 1992; Ochoa-Gaona and Dominguez-Vazquez, 2000; Lobo et al., 2003), with few studies in the temperate forests (Ramirez and Nepamuceno, 1986; Bello, 1994; Olvera et al., 1997). Thus, phenological information for Mexican temperate species is scarce and only partial data can be found in some regional flora or taxonomic monographs where the phenological information comes from records in herbaria specimens rather than periodical field observations.

Understanding phenological patterns and the underlying factors is important in the Monarch Butterfly Biosphere Reserve (MBBR) to help analyze the wide array of biological processes governing forest functions and structure, and also to reflect positive or negative interactions among species (e.g., dispersal of diaspores, population biology of herbivores). Phenological data will also provide valuable information to design sustainable plans for the management and conservation of biodiversity. Specifically, such data will allow to recognize keystone fruit resources in the plant community and will also be useful in planning restoration actions in areas affected by human activities (Chapman et al., 1999; Wallace and Painter, 2002). Unfortunately, deforestation in the MBBR is a major problem that includes a diminished natural resource base for the local people, as well as ecosystem degradation associated with the broad changes in forest cover (Brower et al., 2002; Ramirez et al., 2003).

The purpose of the present study of the reproductive phenology of 112 plant species in the Cerro Altamirano mountain massif in the core zone of the MBBR was threefold: 1) to describe phenological patterns at the community level and within growth forms (annual herbs, perennial herbs, shrubs, and trees); 2) to examine whether or not seasonal variation in rainfall and temperature was correlated with phenophase peaks; and 3) to estimate the degree of individual reproductive synchrony for important woody species. Based on preliminary findings, it was predicted that 1) flowering and fruiting would be triggered by rainfall, 2) growth forms would show different phenological patterns, and 3) woody species would display a pattern of intraspecific synchrony in flowering and fruiting.

Materials and Methods

The study was carried out in one of the three major core zones of the MBBR, the Cerro Altamirano, in the states of Michoacan and Mexico, central Mexico (19[degrees]59'42"-19[degrees]57'07"N and 100[degrees]09'54"-100[degrees]06'39"W), with a surface of 588ha and altitudes of 2500-3320masl (Cornejo et al., 2003). Geologically, this reserve is within the Transmexican Volcanic Belt (Ferrusquia-Villafranca, 1993). The regional climate is temperate-subhumid, with wet summers C([w.sub.1]), an average annual rainfall of 830mm and a mean annual temperature of 15.7[degrees]C (Garcia, 1981). Rainfall is strongly seasonal, with most precipitation occurring from June to September (Figure 1). Vegetation is classified as temperate forest, with two main subtypes: Quercus forest at lower altitudes and Abies forest at higher altitudes (Rzedowski, 1978). The Quercus forest is a floristically rich formation found at 2500-2900masl. In this forest type the most important tree species are Q. castanea Nee and Q. obtusata Humb. & Bonpl. (Fagaceae), and Arbutus xalapensis Kunth (Ericaceae), while the understory contains a great diversity of shrubs and herbs, predominantly Asteraceae, Lamiaceae and Scrophulariaceae. The Abies forest is mostly found above 3000masl, has a canopy dominated by A. religiosa (Kunth) Schltdl. & Chato. (Pinaceae), Q. laurina Humb. & Bonpl. (Fagaceae) and Clethra mexicana DC. (Clethraceae), and an understory of several shrub and herb species (Asteraceae and Lamiaceae; Cornejo-Tenorio et al., 2003).

[FIGURE 1 OMITTED]

Phenological data and analysis

The flowering and fruiting of 112 species were observed in Cerro Altamirano during one year (Jan-Dec 2004), along a transect of approximately 3km that encompassed a 500m elevational gradient, from the lower area at 2500masl to the hill summit at 3000masl. Throughout this path observation sites were established every 100m, for a total of 35 sites. All observations were made during the first week of each month. Each observation site consisted of a 25x4m transect. Based on knowledge of the area (Cornejo et al., 2003), counts were limited to include only the most abundant plant species in the community (Table I): 11 annual herbs, 72 perennial herbs, 21 shrubs, and 8 trees. The presence of open flowers and ripe fruits was recorded only in those species with [greater than or equal to] 10 adult individuals in at least one of the 35 observation sites. In the case of herbs, it was sometimes not possible to define individuals, in which case we recorded flowers or fruits at the level of ramets in no less than 10 sites.

To investigate phenological synchrony of the dominant woody species, 160 mature individuals were marked and observed monthly, belonging to seven tree species (A. religiosa; Arbutus tesellata, A. xalapensis, Ericaceae; Clethra mexicana, Clethraceae; Q. castanea, Q. laurina, and Q. obtusata) and to one shrub species (Arctostaphylos pungens, Ericaceae). Hereafter, this species group was named as tree species. Based in field experience, dominant species were recognized mainly by their numerical abundance. Observations had to be limited to this number of species and individuals for each species due to logistical reasons. However, the distance between individuals of particular species varied from 20 to 50m, depending on their relative abundance and local distribution. The presence of flowers and fruits was observed directly or with the aid of binoculars. Voucher materials of all studied species were deposited in the herbaria of Universidad Nacional Autonoma de Mexico (MEXU) and Instituto de Ecologia (IEB), Mexico.

The flowering and fruiting periods of every species were characterized according to rainfall seasonality (Figure 1) as occurring in the wet (Jun-Sep) or in the dry season (Oct-May). The Pearson's correlation coefficient (Zar, 1999) was used to correlate the number of flowering and fruiting species observed each month against the monthly rainfall A data registered during the study period and mean monthly temperatures (Figure 1). The Rayleigh test (Zar, 1999) was used to assess whether species had flowers or fruits uniformly throughout the year. To calculate the circular statistic parameters, months were converted to angles (0[degrees] for Jan, 30[degrees] for Feb, etc.). The Rayleigh test (z) determines the significance of the mean angle (a), which represents the period of the year throughout which flowering and fruiting is recorded for most species. If z is significant for each reproductive event, then these are concentrated in a specific period of the year, but if z is not significant, it is concluded that the phenophases were distributed uniformly throughout the year. The degree of seasonality for the reproductive activity may be indicated by a vector (R), which is a measure of concentration around the mean angle. The value of the R may vary between 0 and 1, and a high value indicates seasonal phenological behavior; R >0.75 was considered as a high value for this variable.

The activity index (Morellato et al., 1990; Bencke and Morellato, 2002) was used to estimate the synchrony between individuals of each woody species. This index indicates the percentage of individuals during the flowering or fruiting peak of each species. It has three categories: 1) asynchrony, when >20% of the individuals have reproductive structures; 2) low synchrony, when 20-60% when >20% of the individuals have them; and 3) high synchrony, when >60% do so.

Results

Community phenology

All the species monitored flowered and 82% fruited. About 70% of the species flowered during the rainy season and into the beginning of the dry season (Jul-Dec). The mean angle for flowering corresponds to the beginning of September (Figure 2a, Table II). A high proportion of species (73%) produced fruits during the dry season (Oct-May), with a maximum activity at the beginning of November (Figure 2b, Table II). Most species produced flowers and fruits in a specific period of the year. Nevertheless, the low values of R revealed a low degree of reproductive seasonality (Table II). A positive correlation was found among the number of flowering species and rainfall (r= 0.59, P<0.05), whereas for fruiting species the correlation was not significant (r= -0.44, P>0.05). However, for all comparisons performed at the community level and within growth forms against mean monthly temperature, there were no significant differences in flowering or fruiting periods.

Phenology and growth forms

Flowering and fruiting activity in annual and perennial herbs occurred mainly during the rainy season and the beginning of the dry season (Jul-Dec). The number of flowering and fruiting annual herbs was not uniformly distributed throughout the year (Figure 2c-d, Table II). The degree of seasonality denoted by R was high (Table II). The mean angle for flowering species corresponds to the beginning of October, whereas the mean angle for fruiting corresponds to the beginning of November. The number of flowering and fruiting annual herbs was not correlated with rainfall (r= 0.18 and r= 0.33, respectively; P>0.05). Similarly, perennial herbs also show flowering and fruiting in a specific period of the year (Figure 2e-f, Table II); although the degree of seasonality denoted by R was from medium to low (Table II). The mean angle for flowering species was at the beginning of September and the mean angle for fruiting corresponds to the end of October. The number of flowering species was positively correlated with rainfall (r= 0.67, P<0.05), while the correlation for fruiting was not significant (r= 0.23, P>0.05).

[FIGURE 2 OMITTED]

[FIGURE 3 OMITTED]

Shrubs presented flowers and fruits all year long (Figure 2g-h, Table II). Although it was observed that fruiting had two peaks (Apr and Dec, Figure 2c), the R value (0.13) indicated that this phenophase was not seasonal. Only the correlation between the number of fruiting shrubs against the rainfall was statistically significant (r= -0.62, P<0.05).

Trees did not flower uniformly throughout the year and showed a moderate degree of seasonality (Figure 2i, Table II). A large number of species produced flowers during the driest months (Mar-May) and the mean angle of 86[degrees] corresponds to the end of March. The number of fruiting species was distributed homogeneously during the annual cycle, with a low degree of seasonality (Figure 2j, Table II). The correlation between the number of flowering trees and rainfall was not statistically significant (r= -0.42, P>0.05), while for fruiting trees the correlation was negative (r= -0.64, P<0.05).

Intraspecific synchrony in tree species

Flowering of the eight tree species showed a low synchrony in half of the species and high synchrony in the other half (Table III). With regard to fruiting, only A. xalapensis was asynchronic, three species displayed low synchrony, and four species were highly synchronic. Q. laurina was the only species that exhibited a low synchrony in the production of flowers and fruits; on the contrary, A. pungens and C. mexicana were highly synchronic in both phenophases (Figure 3, Table III).

Discussion

Community phenology

The number of species flowering in Cerro Altamirano was positively correlated with rainfall. This result differs from reports for the arboreal, lianas and palms species in the tropical lowland rain forest (Carabias-Lillo and Guevara, 1985; Ibarra-Manriquez et al., 1991; Ibarra-Manriquez, 1992; Ibarra-Manriquez and Oyama, 1992) or tree species in the temperate forest (Ramirez and Nepamuceno, 1986; Olvera et al., 1997), where this phenophase is associated with the season of lower precipitation. These discrepancies are understandable if it is considered that 74% of the species included in the present study are herbs. In fact, the results show that herbs, shrubs, and trees have different phenological patterns, reflecting different responses to environmental factors, particularly to rainfall seasonality, and probably also due to biotic factors such as pollination and dispersai syndromes (see below).

Phenology and growth forms

Several studies have found that flowering activity among herbaceous species is strongly associated to the rainy season (Croat, 1975; Sarmiento and Monasterio, 1983; Batalha and Mantovani, 2000; Spina et al., 2001; Tyler, 2001; Ramirez, 2002; Batalha and Martins, 2004), which agrees with the present findings. The strong relationship between herbs and the rainy season is due to the fact that this life form requires high water availability for their vegetative development and reproduction (Janzen, 1967; Rathcke and Lacey, 1985). Furthermore, in the study site most of the perennial herbs flower earlier than annual species. Ramirez (2002) found the same result and considered that this may be the result of the fact that perennial plants have reserve structures (rhizomes or tubers) that allow them to start their reproductive activity before annual plants. The fact that herbaceous species, the most important growth form in this plant community, produce fewer flowers during the dry season reinforces the argument of Alonso-Mejia et al. (1997), that the potential nectar sources for overwintering monarch butterflies become increasingly unavailable as the dry season advances. Based on their earlier blooming, it is not unexpected that fruiting herbs may also show a peak approximately two months after the maximum flowering season is reached, since this period is required for fruit formation. Fruit ripening has also been associated with the appropriate dispersal season; for instance, diaspores of wind dispersal species ripen during the dry season (Lieberman, 1982; Morellato et al., 1990; Ibarra-Manriquez et al, 1991; Batalha and Martins, 2004), a situation that also occurs in several species of Asteraceae in the study area.

Like other Neotropical localities (Opler et al., 1980; Smith-Ramirez and Armesto, 1994; Batalha and Mantovani, 2000; Spina et al., 2001; Ramirez, 2002; Batalha and Martins, 2004), flowering and fruiting of shrubs was observed during the whole year, even though the greatest number of species presented fruits during the dry season.

This pattern could be explained considering that woody species have a deep root system that allows them to reach available water, or they have water storage structures that buffer the negative impact of seasonal drought (Sarmiento and Monasterio, 1983).

On the other hand, one of the factors proposed to explain flowering activity of trees in the dry season is that wind pollinated species need specific environmental conditions (dry and windy weather) for optimum pollen dispersion (Frankie et al., 1974; Bawa et al., 1985; Ramirez and Nepamuceno, 1986; Bello, 1994; Olvera et al., 1997; Barnes et al., 1998). This argument is useful to explain the present findings, since the wind pollinated trees in the study area (A. religiosa, Q. castanea, Q. laurina, Q. obtusata and S. paradoxa) flower during the driest months of the year (Mar-May; Figures 1 and 3). Fruiting periodicity depends principally on flowering, but it is also influenced by environmental conditions appropriate for fruit development, diaspore dispersal, and seedling establishment (Rathcke and Lacey, 1985; Ibarra-Manriquez et al., 1991; van Schaik et al., 1993). Available information from several Neotropical regions indicate that during the dry season the number of species with anemochorous or autochorous diaspores is higher, while species with zoochorous diaspores seem to produce them most often in the rainy season (Morellato et al., 1990; Ibarra-Manriquez et al., 1991, 2001; Batalha and Mantovani, 2000; Batalha and Martins, 2004). These reproductive patterns were observed in tree species of Cerro Altamirano, where anemochorous and autochorous trees have fruits in the dry season (A. religiosa, C. mexicana, Q. castanea, Q. laurina, Q. obtusata, and S. paradoxa), and zoochorous species fruit mainly in the wet season (A. tessellata and A. xalapensis).

Intraspecific synchrony in tree species

Considering the results of both reproductive cycles, 50% of the woody species showed high synchrony and the other 50% showed low synchrony or asynchrony (Table III). Rabinowitz et al., (1981) found that in comparison with insect-pollinated species, flowering phenology in wind-pollinated plants showed greater intrapopulation synchronization or individuals with shorter flowering times. In Cerro Altamirano, wind-pollinated species (A. religiosa and three species of Quercus) had short periods of flowering, but only A. religiosa was highly synchronic (Figure 3; Table I). Also, A. tesellata, A. pungens, and C. mexicana, which are probably pollinated by diurnal insects (e.g., bees), presented high synchrony during their flowering period, which would allow for the attraction of a higher number of generalist pollinators (Rathcke and Lacey, 1985; Ims, 1990).

From the eight tree species studied, four showed a high fruiting synchrony (Table III). It has been widely proposed in the literature that the mast fruiting effect leads to satiation of specialist and generalist predators, which allows for a part of the fruit crop to escape predation (Rathcke and Lacey, 1985; Crawley, 2000 and references therein). This event probably occurred in Q. castanea and Q. laurina. Both oak species had a high fruit production during 2004 but also showed many damaged nuts, probably by squirrels or mice. Mast fruiting in oak species is a widely documented phenological behavior in other localities of temperate forest and has been considered as an evolved reproductive strategy, because it is not simply a response to weather conditions (Sork et al., 1993; Kelly anal Sork, 2002).

Conclusions

The results obtained indicate that the reproductive phenology patterns of the temperate flora of Cerro Altamirano are similar to those documented for seasonal tropical communities. Nevertheless, it is necessary to perform phenological studies in the other core zones of the reserve, with the purpose of contrasting the findings and to obtain long-term data. This last issue has special significance as temporal changes in plant resources profoundly affect animals, and also because cycles of plant reproduction are crucial for an understanding of ecosystem functioning (Rathcke and Lacey, 1985; van Schaik et al., 1993; Barnes et al., 1998; Chapman et al., 1999; Poulin et al., 1999; Wallace and Painter, 2002). Furthermore, it has been detected that the reproductive season of particular species may change through the years and also that many species have multiyear reproductive cycles (Frankie et al., 1974; Bawa et al., 1985; Ibarra-Manriquez et al., 1991; Newstrom et al., 1994; Chapman et al., 1999). In fact, recently (Oct-Dec 2006) a high number of reproductive A. religiosa trees were detected in each one of the three core zones of the MBBR, a condition never observed along the previous six years of floristic inventory. This situation suggests that A. religiosa could be considered as a supra-annual flowering species, (sensu Newstrom et al., 1994), but in order to confirm this hypothesis long-term phenological observations (at least 12 years; Newstrom et al., 1994) are needed.

Another important point to extend phenological studies to other areas of the reserve is that the floristic composition of each core zone (Cerro Altamirano, Chincua-Campanario-Chivati, and Cerro Pelon) is very particular and each should be considered as a distinct plant community. The floristic inventory carried out in these sanctuaries reached around 650 species (2000-2006), of which only -14% (92 species) was shared in all three areas (Ibarra-Manriquez, unpublished data). In fact, Cerro Altamirano area has 213 species (33%) registered exclusively in its forests. Consequently, phenological information must be generated for other species that inhabit these temperate forests together with monarch butterflies. For implementing restoration actions to recover disturbed areas near overwintering sites, or for degraded ground recovery, the information obtained should be a guide to know the appropriate timing for collecting mature seeds of several species (e.g., A. religiosa, Ceanothus coeruleus, Lupinus spp., Quercus spp.).

Finally, it would be advisable that the reproductive phenology of plants in temperate forests of Mexico be addressed in a more comprehensive way, where phenological patterns could be related to other reproductive attributes, such as pollination syndromes and seed dispersai or sexual systems (monoecious, dioicious or hermaphroditic). A better understanding of phenological patterns at both the level of species and of ecosystems is crucial for the management and long terra conservation of ecosystems (Newstrom et al., 1994; Joshi and Janarthanam, 2004). A better habitat management of existing overwintering sites and buffer areas in the MBBR is a critical element for the preservation of the mass of wintering aggregations of monarch butterflies in Mexico, an exceptional biological phenomenon highly threatened by human activities (Brower et al., 2002; Ramirez et al., 2003).

ACKNOWLEDGMENTS

The authors acknowledge the careful and extensive revision and edition of this paper by Lincoln B. Brower, and thank Ellen Andresen and William C. Burger for criticism of earlier version of the manuscript, Juan Martinez-Cruz, Fernando Pineda-Garcia, Miguel Angel Salinas-Melgoza and Roberto Sayago-Lorenzana for their help in the field work. The first author received a scholarship from the Consejo Nacional de Ciencia y Tecnologia (CONACyT; No 181848).

Received: 04/03/2007. Modified: 05/30/2007. Accepted: 06/06/2007.

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Guadalupe Cornejo-Tenorio. M.Sc. in Biological Sciences, Universidad Nacional Autonoma de Mexico (UNAM). Researcher, UNAM, Morelia, Mexico. e-mail: gcornejo@oikos.unam.mx

Guillermo Ibarra-Manriquez. Ph.D. in Biology, UNAM, Mexico. Investigador, UNAM, Mexico Address: Centro de Investigaciones en Ecosistemas, UNAM. Antigua Carretera a Patzcuaro No 8701, Col. San Jose de la Huerta, 58190 Morelia, Michoacan, Mexico. e-mail: gibarra@oikos.unam.mx
TABLE I
FLOWERING AND FRUITING PHENOLOGIES OF 112 SPECIES FROM CERRO
ALTAMIRANO, ONE OF THE CORE ZONES OF THE MONARCH BUTTERFLY
BIOSPHERE RESERVE IN CENTRAL MEXICO

Taxa                                   Growth form

Apiaceae
  Donnellsmithia juncea (Humb.
    & Bonpl.) Math. & Constance       Perennial herb
  Tauschia alpina (Coult. & Rose)
    Math.                             Perennial herb
Asteraceae
  Acourtia turbinata (Lox.)
    Reveal & King                     Perennial herb
  Ageratina areolaris (DC.) Gage          Shrub
  A. glabrata (Kunth) RM King & H
    Rob.                                  Shrub
  A. mairetiana (DC.) RM King & H
    Rob. var. mairetiana                  Shrub
  A. pazcuarensis (Kunth) R.M.
    King. & H. Rob.                   Perennial herb
  A. petiolaris (Moc. ex DC.)
    R.M. King & H. Rob.                   Shrub
  Archibaccharis hirtella (DC.)
    Heering                               Shrub
  A. serratifolia (Kunth) S.F.
    Blake                             Perennial herb
  Artemisia ludoviciana Nutt.         Perennial herb
  Baccharis conferta Kunth                Shrub
  B. pteronioides DC.                 Perennial herb
  Bidens odorata Cav.                  Annual herb
  Cosmos parviflorus (Jacq.) Kunth     Annual herb
  C. scabiosoides Kunth               Perennial herb
  Dahlia coccinea Cav.                Perennial herb
  D. scapigera (A. Dietr.) Knowles
    & Westc.                          Perennial herb
  Dyssodia papposa (Vent.) Hitchc.     Annual herb
  D. pinnata (Cav.) B.L. Rob. var.
    pinnata                            Annual herb
  Galinsoga quadriradiata Ruiz &
    Pav.                               Annual herb
  Hieracium dysonymum Blake           Perennial herb
  Jaegeria hirta (Lag.) Less.         Perennial herb
  Laennecia schiedeana (Less.)
    G.L. Nesom                         Annual herb
  Montanoa grandiflora DC.                Shrub
  Packera sanguisorbae (DC.)
    C. Jeffrey                        Perennial herb
  Piqueria trinervia Cav.             Perennial herb
  Roldana barba-johannis (DC.)
    H. Rob. & Brettell                    Shrub
  Stevia elatior Knuth                Perennial herb
  S. monardifolia Kunth               Perennial herb
  S. salicifolia Cav. var.
    salicifolia                           Shrub
  S. serrata Cav. var. serrata        Perennial herb
  Tagetes lucida Cav.                 Perennial herb
  T. lunulata Ortega                   Annual herb
  T. micrantha Cav.                    Annual herb
  Verbesina oncophora B.L. Rob.
    & Greenm.                             Shrub
  Viguiera hemsleyana S.F. Blake      Perennial herb
  Viguiera sessilifolia DC.           Perennial herb
Boraginaceae
  Lithospermum distichum Ortega       Perennial herb
Bromeliaceae
  Tillandsia andrieuxii (Mez)
    L.B. Sm.                          Perennial herb
Campanulaceae
  Diastatea micrantha (Kunth)
    McVaugh                            Annual herb
  Lobelia gruina Cav.                 Perennial herb
Caprifoliaceae
  Symphoricarpos microphyllus Kunth       Shrub
Caryophyllaceae
  Arenaria bourgaei Hemsl.            Perennial herb
Cistaceae
  Helianthemum glomeratum Lag.
    ex DC.                            Perennial herb
Clethraceae
  Clethra mexicana DC.                     Tree
Clusiaceae
  Hypericum silenoides Juss.
    var. silenoides                   Perennial herb
Commelinaceae
  Commelina coelestis Willd.          Perennial herb
  Gibasis pulchella (Kunth) Raf.      Perennial herb
Ericaceae
  Arbutus tessellata P.D. Sorensen         Tree
  A. xalapensis Kunth                      Tree
  Arctostaphylos pungens Kunth            Shrub
  Comarostaphylis discolor (Hook.)
    Diggs subsp. rupestris                Shrub
Fabaceae
  Cologania biloba (Lindl.)
    G. Nicholson                      Perennial herb
  Desmodium neo-mexicanum A. Gray     Perennial herb
  Lathyrus parviflorus S. Watson      Perennial herb
  Lupinus montanus Kunth              Perennial herb
  Phaseolus pluriflorus Marechal,
    Mascherpa & Stainier              Perennial herb
Fagaceae
  Quercus castanea Nee                     Tree
  Q. laurina Humb. & Bonpl.                Tree
  Q. obtusata Humb. & Bonpl.               Tree
Gentianaceae
  Gentiana spathacea Kunth            Perennial herb
  Halenia brevicornis (Kunth)
    G. Don                            Perennial herb
  H. plantaginea (Kunth) Griseb.      Perennial herb
Geraniaceae
  Geranium potentillaefolium DC.      Perennial herb
  G. seemanni Peyr.                   Perennial herb
Hypoxidaceae
  Hypoxis mexicana Schult. &
    Schult. f.                        Perennial herb
Iridaceae
  Sisyrinchium convolutum Nocca       Perennial herb
Lamiaceae
  Lepechinia caulescens (Ortega)
    Epling                            Perennial herb
  Salvia amarissima Ort.              Perennial herb
  S. elegans Vahl                     Perennial herb
  S. fulgens Cav.                     Perennial herb
  S. laevis Benth.                    Perennial herb
  S. lavanduloides Benth.             Perennial herb
  S. mexicana L. var. mexicana        Perennial herb
  S. patens Cav.                      Perennial herb
  Scutellaria caerulea Sesse & Moc.   Perennial herb
  Stachys parvifolia M. Martens &
    Galeotti                          Perennial herb
Lentiburaliaceae
  Pinguicula moranensis Kunth         Perennial herb
Lythraceae
  Cuphea aequipetala Cav.             Perennial herb
Onagraceae
  Fuchsia thymifolia Kunth                Shrub
  Lopezia racemosa Cav.                Annual herb
Orchidaceae
  Corallorrhiza odontorhiza
    (Willd.) Nutt.                    Perennial herb
  Govenia capitata Lindl.             Perennial herb
Orobanchaceae
  Conopholis alpina Liebm.            Perennial herb
Pinaceae
  Abies religiosa (Kunth)
    Schltdl. & Cham.                       Tree
Polemoniaceae
  Loeselia mexicana (Lam.) Brand      Perennial herb
Polygalaceae
  Monnina ciliolata DC.                   Shrub
Ranunculaceae
  Clematis dioica L.                      Shrub
  Ranunculus petiolaris Kunth ex
    DC. var. arsenei (Benson) T
    Duncan                            Perennial herb
Rhamnaceae
  Ceanothus coeruleus Lag.                Shrub
Rosaceae
  Alchemilla procumbens Rose          Perennial herb
Rubiaceae
  Bouvardia longiflora (Cav.) Kunth       Shrub
  B. ternifolia (Cav.) Schltdl.       Perennial herb
  Crusea longiflora (Willd. ex
    Roem. & Schult.) WR Anderson       Annual herb
  Galium aschenbornii Nees & S.
    Schauer                           Perennial herb
Salicaceae
  Salix paradoxa Kunth                     Tree
Scrophulariaceae
  Castilleja tenuiflora Benth.        Perennial herb
  Lamourouxia dasyantha
    (Cham. & Schltdl.) Ernst          Perennial herb
  L. multifida Kunth                  Perennial herb
  Mecardonia procumbens (Mill.)
    Small                             Perennial herb
  Penstemon roseus (Cerv. ex Sweet)
    G Don                             Perennial herb
Solanaceae
  Cestrum thyrsoideum Kunth               Shrub
  Physalis orizabae Don               Perennial herb
  Solanum demissum Lindl.             Perennial herb
Valerianaceae
  Valeriana barbareifolia M.
    Martens & Galeotti                Perennial herb
Verbenaceae
  Glandularia teucriifolia
    (M. Martens & Galeotti) Umber     Perennial herb
  V. recta Kunth                      Perennial herb
Violaceae
  Viola humilis Kunth                 Perennial herb
  V. painteri Rouse & House           Perennial herb
Viscaceae
  Cladocolea diversifolia (Benth.)
    Kuijt                                 Shrub
  Phoradendron schumanni Trel.            Shrub

               Taxa                     Flowering         Fruiting

Apiaceae
  Donnellsmithia juncea (Humb.
    & Bonpl.) Math. & Constance            9-10              11
  Tauschia alpina (Coult. & Rose)
    Math.                                5-8, 10             8-9
Asteraceae
  Acourtia turbinata (Lox.)
    Reveal & King                          1-3                3
  Ageratina areolaris (DC.) Gage         1, 10-12         1, 11-12
  A. glabrata (Kunth) RM King & H
    Rob.                                   2-4               4-5
  A. mairetiana (DC.) RM King & H
    Rob. var. mairetiana                 1-5, 12             2-6
  A. pazcuarensis (Kunth) R.M.
    King. & H. Rob.                       10-12              --
  A. petiolaris (Moc. ex DC.)
    R.M. King & H. Rob.                    2-4               3-6
  Archibaccharis hirtella (DC.)
    Heering                             1-3, 11-12           3-5
  A. serratifolia (Kunth) S.F.
    Blake                               1-4, 11-12         3-5, 12
  Artemisia ludoviciana Nutt.             10-12              12
  Baccharis conferta Kunth                 3-6               4-7
  B. pteronioides DC.                      5-6                7
  Bidens odorata Cav.                     10-12             10-12
  Cosmos parviflorus (Jacq.) Kunth          9               10-11
  C. scabiosoides Kunth                    8-10              --
  Dahlia coccinea Cav.                     8-9              10-11
  D. scapigera (A. Dietr.) Knowles
    & Westc.                               8-9              10-11
  Dyssodia papposa (Vent.) Hitchc.         9-10              12
  D. pinnata (Cav.) B.L. Rob. var.
    pinnata                                 10              10-12
  Galinsoga quadriradiata Ruiz &
    Pav.                                    10              10-12
  Hieracium dysonymum Blake                3-5               5-6
  Jaegeria hirta (Lag.) Less.             10-11             10-12
  Laennecia schiedeana (Less.)
    G.L. Nesom                            10-11              12
  Montanoa grandiflora DC.                 9-10             1, 12
  Packera sanguisorbae (DC.)
    C. Jeffrey                             2-6               5-7
  Piqueria trinervia Cav.                  8-12             10-12
  Roldana barba-johannis (DC.)
    H. Rob. & Brettell                   1-2, 12             3-4
  Stevia elatior Knuth                     8-9              9-12
  S. monardifolia Kunth                  1, 8-12            10-12
  S. salicifolia Cav. var.
    salicifolia                          1, 10-12          1-4, 12
  S. serrata Cav. var. serrata             8-12             10-12
  Tagetes lucida Cav.                      8-12              12
  T. lunulata Ortega                       9-12             10-12
  T. micrantha Cav.                        8-9              10-12
  Verbesina oncophora B.L. Rob.
    & Greenm.                             1, 12              --
  Viguiera hemsleyana S.F. Blake           9-10             10-11
  Viguiera sessilifolia DC.                9-10             11-12
Boraginaceae
  Lithospermum distichum Ortega            6-8               8-9
Bromeliaceae
  Tillandsia andrieuxii (Mez)
    L.B. Sm.                               5-7             5, 8-12
Campanulaceae
  Diastatea micrantha (Kunth)
    McVaugh                               10-12              --
  Lobelia gruina Cav.                    1, 9-12             --
Caprifoliaceae
  Symphoricarpos microphyllus Kunth        7-9              10-12
Caryophyllaceae
  Arenaria bourgaei Hemsl.                 5-10             5-12
Cistaceae
  Helianthemum glomeratum Lag.
    ex DC.                              1-4, 8-12         2-5,8-12
Clethraceae
  Clethra mexicana DC.                     1-2               3-4
Clusiaceae
  Hypericum silenoides Juss.
    var. silenoides                        8-12             9-12
Commelinaceae
  Commelina coelestis Willd.               8-9               10
  Gibasis pulchella (Kunth) Raf.           7-10              --
Ericaceae
  Arbutus tessellata P.D. Sorensen      1-9, 11-12           5-6
  A. xalapensis Kunth                      3-6              7-12
  Arctostaphylos pungens Kunth             1-12             4-10
  Comarostaphylis discolor (Hook.)
    Diggs subsp. rupestris                2, 4-9       1-2, 5-6, 11-12
Fabaceae
  Cologania biloba (Lindl.)
    G. Nicholson                           8-10              --
  Desmodium neo-mexicanum A. Gray          9-10              --
  Lathyrus parviflorus S. Watson           7-9               --
  Lupinus montanus Kunth                1-3, 10-12           1-5
  Phaseolus pluriflorus Marechal,
    Mascherpa & Stainier                   8-9               --
Fagaceae
  Quercus castanea Nee                     3-5             1-4, 12
  Q. laurina Humb. & Bonpl.                4-5               12
  Q. obtusata Humb. & Bonpl.               3-5              11-12
Gentianaceae
  Gentiana spathacea Kunth               l-2, 12             2-3
  Halenia brevicornis (Kunth)
    G. Don                                  11               --
  H. plantaginea (Kunth) Griseb.            11               --
Geraniaceae
  Geranium potentillaefolium DC.           6-8                9
  G. seemanni Peyr.                        7-8                9
Hypoxidaceae
  Hypoxis mexicana Schult. &
    Schult. f.                             8-9                9
Iridaceae
  Sisyrinchium convolutum Nocca            7-9               10
Lamiaceae
  Lepechinia caulescens (Ortega)
    Epling                                 8-9               10
  Salvia amarissima Ort.                   8-12              --
  S. elegans Vahl                       1-5, 10-12           3-5
  S. fulgens Cav.                          7-12             10-12
  S. laevis Benth.                         9-12              12
  S. lavanduloides Benth.                1, 7-12         2-4, 10-12
  S. mexicana L. var. mexicana             8-12          1-4, 10-12
  S. patens Cav.                           8-11              --
  Scutellaria caerulea Sesse & Moc.        7-10             10-11
  Stachys parvifolia M. Martens &
    Galeotti                               7-9               8-9
Lentiburaliaceae
  Pinguicula moranensis Kunth              5-9               10
Lythraceae
  Cuphea aequipetala Cav.                  7-10             8-11
Onagraceae
  Fuchsia thymifolia Kunth                 5-9              10-12
  Lopezia racemosa Cav.                  1, 9-12              2
Orchidaceae
  Corallorrhiza odontorhiza
    (Willd.) Nutt.                         7-8               --
  Govenia capitata Lindl.                  6-9              11-12
Orobanchaceae
  Conopholis alpina Liebm.                 4-5               5-7
Pinaceae
  Abies religiosa (Kunth)
    Schltdl. & Cham.                       3-5               1-4
Polemoniaceae
  Loeselia mexicana (Lam.) Brand        1-2, 10-12           --
Polygalaceae
  Monnina ciliolata DC.                   1, 8-9            11-12
Ranunculaceae
  Clematis dioica L.                       5-10               1
  Ranunculus petiolaris Kunth ex
    DC. var. arsenei (Benson) T
    Duncan                                 6-10             9-11
Rhamnaceae
  Ceanothus coeruleus Lag.            1, 4-8, 10-12           1
Rosaceae
  Alchemilla procumbens Rose               7-12              --
Rubiaceae
  Bouvardia longiflora (Cav.) Kunth        4-10              12
  B. ternifolia (Cav.) Schltdl.            4-10           1, 10-12
  Crusea longiflora (Willd. ex
    Roem. & Schult.) WR Anderson           8-10              --
  Galium aschenbornii Nees & S.
    Schauer                                7-9           1-2, 10-12
Salicaceae
  Salix paradoxa Kunth                      3                 5
Scrophulariaceae
  Castilleja tenuiflora Benth.             1-12            2-3, 10
  Lamourouxia dasyantha
    (Cham. & Schltdl.) Ernst              11-12              12
  L. multifida Kunth                       9-12             10-12
  Mecardonia procumbens (Mill.)
    Small                                  8-10             10-12
  Penstemon roseus (Cerv. ex Sweet)
    G Don                                  7-12          1-2, 10-12
Solanaceae
  Cestrum thyrsoideum Kunth             1-2, 9-11            --
  Physalis orizabae Don                    7-9                9
  Solanum demissum Lindl.                  7-8               --
Valerianaceae
  Valeriana barbareifolia M.
    Martens & Galeotti                     7-10             10-12
Verbenaceae
  Glandularia teucriifolia
    (M. Martens & Galeotti) Umber          6-9               8-9
  V. recta Kunth                           8-10              10
Violaceae
  Viola humilis Kunth                      6-9               10
  V. painteri Rouse & House                5-9                9
Viscaceae
  Cladocolea diversifolia (Benth.)
    Kuijt                                  4-5               3-4
  Phoradendron schumanni Trel.              5               5-10

Months are indicated by numbers. Hyphens or commas between
months means continual or intermittent phenological activity,
respectively.

TABLE II
VALUES OF CIRCULAR STATISTIC ANALYSES FOR FLOWERING
AND FRUITING SPECIES IN CERRO ALTAMIRANO CORE ZONE

                    Rayleigh      Degree of       Mean angle
                    test (z)   seasonality (R)
Flowering
  Community         32.37 *         0.27         245 [degrees]
  Annual herbs      17.35 *         0.80         275 [degrees]
  Perennial herbs   50.28 *         0.42         241 [degrees]
  Shrubs             0.02 ns        0.01              --
  Trees              8.49 *         0.54          86 [degrees]
Fruiting
  Community         11.32 *         0.16         308 [degrees]
  Annual herbs      14.88 *         0.74         304 [degrees]
  Perennial herbs   12.72 *         0.21         292 [degrees]
  Shrubs            1.55 ns         0.13              --
  Trees             0.91 ns         0.18              --

* P < 0.001.

TABLE III
DEGREE OF INTRASPECIFIC
SYNCHRONY * IN FLOWERING AND
FRUITING AS PERCENTAGE OF
INDIVIDUALS FOR EIGHT WOODY
SPECIES OF CERRO ALTAMIRANO
CORE ZONE

Species                  Flowering   Fruiting

Abies religiosa             90          50
Arbutus tessellata          80          25
Arbutus xalapensis          40          15
Arctostaphylos pungens      95          95
Clethra mexicana            70          70
Quercus castanea            40          90
Quercus laurina             60          30
Quercus obtusata            50          75

* Synchrony categories: asynchrony (<20% of
individuals with flowers or fruits), low synchrony
(20-60%) and high synchrony (>60%). n = 20 for
each species.
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Author:Cornejo-Tenorio, Guadalupe; Ibarra-Manriquez, Guillermo
Publication:Interciencia
Date:Jul 1, 2007
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