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.
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 /
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.
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.
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).
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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.
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).
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).
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).
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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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.