Introduction

Some authors document that plant populations and species have evolved response mechanisms to environmental signals that stimulate the development of vegetative and reproductive structures (^{Hamann, 2004}; ^{Elzinga et al., 2007}), which together generate the behavior at the community level. The environmental triggers to which the flowering and fruiting patterns of tree taxa respond are varied and differ depending on the ecosystem in question: while in temperate zones, the species respond to obvious factors such as photoperiod and temperature (^{Tooke and Battey, 2010}; ^{Diez et al., 2012}), in tropical regions, they react to the variation of atmospheric and soil humidity, as well as to the incidence of solar radiation (^{Hamann, 2004}; ^{Ochoa et al., 2008}).

The presence of water, through rainfall, exerts a strong influence on phenology in tropical ecosystems, but its effect has a different degree of importance in those with high moisture content and in dry ecosystems. Furthermore, it is relevant how humidity is distributed throughout the year, generating differentiated phenological behaviors in ecosystems (^{Acevedo and Hernández, 2013}).

Researchers agree that complex evolutionary processes have led species to coincide in their flowering times, in response to environmental factors that increase the probability of their reproduction; among them, abiotic factors such as precipitation, temperature, photoperiod, and biotic factors such as the presence of pollinators, herbivores, etc. (^{Janzen, 1967}).

In dry and humid seasonal neotropical forests, there is a tendency for the richness and abundance of flowering tree species to be concentrated in the dry season or periods of lower humidity (^{Janzen, 1967}; ^{Williams and Meave, 2002}; ^{Cortés-Flores et al., 2019}), a pattern that is registered also for some mesophilic mountain forests in Mexico (^{Hernández and Carreón, 1987}; ^{Solórzano et al., 2010}); however, for some neotropical temperate forests, photoperiod is one of the most influential elements in the floral phenology of woody taxa (^{Cortés-Flores et al., 2015}).

Fruit production is expected to occur there where the best soil moisture conditions for the diaspores prevail, allowing the seeds to germinate and grow sufficiently in their underground and aerial parts to enable them to survive during the first dry season of the year (^{van Schaik et al., 1993}; ^{Hamann, 2004}; ^{Zimmerman et al., 2007}). Among the patterns observed in fruiting at the community level in dry tropical forests, certain species bear fruit at the dry-rainy season interface (^{Smythe, 1970}), and the fruits germinating in the immediately subsequent rainy season (recalcitrant seeded taxa); while in other species, fruiting occurs at the end of the rainy season, and their diaspores, which usually have dormancy mechanisms of months (species with orthodox seeds), germinate until the next wet season or in the following wet seasons (^{González et al., 2016}; ^{Topete et al., 2020}).

In tropical forests, with little or no seasonality, the flowering and fruiting patterns of tree species seem to respond to the incidence of solar radiation (^{Hamann, 2004}; ^{Zimmerman et al., 2007}); while, in Mexican temperate forests, day length has a positive effect on floral phenology (^{Cortés-Flores et al., 2015}).

Understanding flowering and fruiting behavior in different ecosystems helps to explain the patterns that govern the distribution and abundance of animal groups (^{Newstom et al., 1994}); is also relevant for determining the optimal time for collecting diaspores for propagation purposes (^{Brennan, 1996}; ^{Ochoa et al., 2008}).

The purpose of this research was to describe the reproductive phenology, flowering and fruiting, at the community level, of tree species existing in a mountainous area of Western Mexico with high environmental heterogeneity. For this purpose, the following questions were addressed: How does the flowering and fruiting of tree species vary within the annual cycle at the community level? Are there differences in flowering and fruiting patterns between existing plant communities and with terrain altitude? Is there any correlation between flowering and fruiting patterns with temperature, precipitation, evaporation, relative humidity and solar radiation?

Materials and Methods

Study area

The research was carried out in a mountainous area of the Sierra Madre del Sur, an area comprising a 6 × 6 km quadrangle, with an area of 3 600 ha and an altitudinal gradient of 1 500 to 2 250 masl. The quadrangle is located between the coordinates 19°34'14"-19°37'30" N and 104°14'49"-104°18'16" W, in the municipalities of Autlán de Navarro and Cuautitlán de García Barragán in the state of Jalisco, and, within its boundaries, it is located the Las Joyas Scientific Station (ECLJ) (^{Jardel et al., 2004}). The ECLJ is a property owned by the Government of the State of Jalisco and is part of the Manantlán-Las Joyas core zone in the Sierra de Manantlán Biosphere Reserve, Jalisco (^{Jardel et al., 2004}). The center of the LJCS is located 22 km south-southeast of the city of Autlán de la Grana, 17 km east of Casimiro Castillo and 52 km north of the port of Manzanillo.

The vegetation corresponds to mesophilic mountain forest (MMF), Pinus forest (PF), Quercus forest (QF), gallery forest (GF), Pinus-Quercus forest (PQF), secondary vegetation (SV), pine shoot (PS), grassland and agricultural land (GA), and rock outcropping and erosion (RE) (^{Jardel et al., 2004}). Since 1985, the ECLJ has been exempt from disturbances such as agriculture, livestock and forestry harvesting; however, some surface fires and the occurrence of cyclones such as Jova and Patricia in 2011 and 2015, respectively, eventually occur. The climate is markedly seasonal, with a cold season from October to January, a dry season from February to May and a rainy season from June to September. Based on the climatic records of the last 30 years, the average annual temperature and precipitation have been 15.5 °C and 1 663 mm, respectively; according to information from the local weather station (Figure 1).

Precipitación = Precipitation; Meses = Months; Temperatura = Temperature.

Figure 1 Climatogram of the ECLJ, constructed with information from 1993-2019, registered in the climatological station of the Station, located at 1 850 masl. 

Results

Flowering and fruiting of tree species at the community level

Of the 3 000 specimens examined, only 1 724 met the criteria to be considered as flowering or fruiting according to the definition of the method. 124 species, 96 genera, and 49 families of tree species were registered. The families with the most specimens were Fagaceae, with 181 (10.50 %); Solanaceae, with 130 (7.54 %); Fabaceae, with 102 (5.92 %); Malvaceae,with 88 (5.10 %), and Betulaceae, with 74 (4.29 %). The flowering of tree taxa in the study area exhibited a bimodal distribution pattern, with one flowering peak in March-May and another in November-January, and a noticeable decrease in the number of species from August to October, although taxa were flowering all year round (Figure 2). As for fruiting, it was richest from February to July, with a decrease from August to November, but fruiting taxa were present throughout the year (Figure 2).

Riqueza de especies = Species richness; Meses = Months; Floración = Flowering; Fructificación =Fruiting.

Figure 2 Richness of flowering and fruiting species during the year. 

The richness of flowering species was higher in the dry season; there were no significant statistical differences regarding the cold season, (F= 13.02, gl=2, p≤0.0022) (Figure 3a). The highest richness of fruiting species occurred in the dry season and was statistically different from the cold and rainy seasons (F= 5.46, gl= 2, p≤0.0280) (Figure 3b).

Especies en floración = Species in flowering; Especies en fructificación = Species in fruiting; Estaciones = Seasons; Fría = Cold; Seca = Dry; Lluviosa = Rainy. Different letters indicate significant differences at a p≤0.05.

Figure 3 a. Richness of flowering species by season; b. Richness of fruiting species by season. 

Flowering and fruiting patterns by plant community

The MMF was the community with the highest number of flowering and fruiting specimens and where the greatest richness of families, genera, and species was identified; while the lowest richness of taxa and specimens was observed in the GF (Table 1).

Table 1 Register of specimens by plant communities and their richness of taxa. 

Vegetation	Sflowers	Sfruits	Species	Genera	Families
GF	94	77	41	38	28
SV	101	92	46	39	26
PF	127	148	63	48	31
PQF	159	118	64	49	26
QF	161	168	76	54	32
MMF	397	383	115	91	47

GF = Gallery forest; SV = Secondary vegetation; PF = Pinus forest; PQF = Pinus-Quercus forest; QF = Quercus forest; MMF = Mesophilic mountain forest; Sflowers = registered specimens with flowers; Sfruits = registered specimens with fruits.

The flowering pattern by plant community was consistent with the one registered for tree species as a whole. There is a peak in the concentration of richness of flowering species from February to May, and another, from November to December, with some small variations in the PF, where the number of flowering species exhibited a notorious increase from December to March; while in the QF, the first peak of flowering was observed in March and April, and the second, from November to January (Figure 4).

VS = Secondary vegetation; BQ = Quercus forest; BPQ = Pinus-Quercus forest; BP = Pinus forest; BMM = Mesophilic mountain forest; BG = Gallery forest. Especies en floración = Species in flowering; Meses = Months.

Figure 4 Flowering patterns by plant communities. 

Fruiting by plant community is a little more heterogeneous in its behavior while tending to the fruiting pattern exhibited by all taxa. Greater richness of fruiting species was observed from February to July, with a decrease from August to October, and an increase in November and December (Figure 5).

VS = Secondary vegetation; BQ = Quercus forest; BPQ = Pinus-Quercus forest; BP = Pinus forest; BMM = Mesophilic mountain forest; BG = Gallery forest. Especies en fructificación = Species in fruiting; Meses = Months.

Figure 5 Fruiting patterns by plant communities. 

Flowering and fruiting patterns across the altitudinal gradients

The richness of flowering and fruiting species was greatest at the altitude range of 1 700 to 2 000 masl, with a very noticeable drop above 2 100 masl (Figure 6).

Gradiente elevacional = Altitudinal gradients; Riqueza de especies = Species richness; Floración = Flowering; Fructificación = Fruiting.

1 = 1 500-1 600; 2 = 1 600-1 700; 8 = 2200-2300 masl.

Figure 6 Species distribution by altitudinal gradients. 

Discussion

Certain authors have documented (^{Williams and Meave, 2002}; ^{Solórzano et al., 2010}) the limitations of the use of herbarium specimens in studies of reproductive phenology, including the absence of a record of the intensity of the phenophases and of the abundance of individuals in flowering or fruiting, or the fact that this is very limited and differentiated among species. In addition, abundant and continuous collections in an area over several years are required in order to obtain a good representation of the phenology of the species. Except for the first two limitations, the continuous collection of botanical material during more than 30 years at the ECLJ and the surrounding areas allows a good degree of confidence in the patterns of reproductive phenology determined at the community level and by vegetation type.

The 124 tree species recorded for the ECLJ represent 27 % of this biological form in the Sierra of Manantlán (^{Vázquez et al., 1995}). The families with the most flowering or fruiting specimens corresponded to those with the greatest richness of tree species at the ECLJ (^{Cuevas et al., 2004}; ^{Cuevas et al., 2021}).

The flowering pattern registered at the ECLJ, exhibiting a greater richness of flowering tree species during the dry season (Figures 2, 3a), is in line with what has been reported in seasonal humid tropical forests and in temperate forests (^{Janzen, 1967}; ^{Reich and Borchert, 1984}; ^{Wright and van Schaik, 1994}; ^{Moore, 2008}; ^{Ochoa et al., 2008}; ^{Cortés-Flores et al., 2015}), as well as in mesophilic forests of Mexico (^{Hernández and Carreón, 1987}; ^{Solórzano et al., 2010}). This pattern may be attributed to the fact that during this period the species are less photosynthetically active, after the rainy season, which allowed the accumulation of reserves (^{Singh and Kushwaha, 2006}); furthermore, there is a lower incidence of insect pests during the dry season (^{Wright and van Schaik, 1994}).

There is another set of factors that may exert an influence, some of which have been pointed out by other authors (^{Janzen, 1967}; ^{Moore, 2008}); they include the abundance of certain groups of pollinators, mainly honeybees and bees; the absence or decrease in the number of leaves renders the flowers more visible to pollinators; the flowers do not fall, nor does their nectar concentration diminish, because of the rains. The importance of the insect group as pollinators appears to be supported, since, based on the available information (^{Cuevas et al., 2021}), and according to the types of flowers, it is suggested that 74 % of the tree species in the area exhibit entomophilous pollination syndromes, while pollination is anemophilous in 21 %, and ornithophilous in 5 %.

Fruiting is at its richest from February to July, coinciding with most of the dry season and the beginning of the rainy season, with a noticeable decrease in the months with more precipitation (Figures 2, 3b) ―a previously registered pattern (^{Hamann, 2004}; ^{Cornejo and Ibarra, 2007}; ^{Solórzano et al., 2010}). This has been explained as logical, in the sense that fruit production in the dry season and the onset of rainfall minimizes seed exposure to predators and provides time for diaspores to germinate and seedling establishment to occur more successfully, since it profits from the moisture available in the environment during the short rainy season, especially in the soil (^{Hamann, 2004}; ^{Singh and Kushwaha, 2006}).

Species that exhibit their fruiting peaks at the end of the rainy season possibly have diaspores with dormancy periods, which should allow them to be viable until the next rainy season.

Given that there are 20 or more flowering and fruiting species in the months with the least richness (Figure 2) although the area has clear seasonal rainy and dry seasons, as well as a cold period, it is considered that the mountain area of western Mexico has a higher humidity in the environment than dry tropical regions, which generates conditions for the presence of species with reproductive structures throughout the year. This coincides with what has been reported in other studies for Mexico, where the predominant vegetation is mountain mesophilic forest (^{Hernández and Carreón, 1987}; ^{Solórzano et al., 2010}).

It is important to consider that, in the plant communities of the area, the presence of organic matter in the soil should contribute to the maintenance of soil moisture, which generates conditions for the tree species to be evergreen or deciduous for short periods, with the existence of a certain degree of photosynthetic activity, and, therefore, flowering and fruiting species are observed throughout the year.

The rebound in the richness of flowering and fruiting species observed from October to December (Figure 2) could correspond to a decrease in precipitation starting in October (Figure 1). The decrease in the richness of flowering and fruiting species in January would be the result of a drop in temperature or a lower incidence of specimen collection in that month.

The richness of flowering and fruiting species was higher in the MMF (Figures 4, 5; Table 1), which was expected, given that this plant community has the largest wealth of tree species in the world (^{Cuevas et al., 2004}; ^{Cuevas et al., 2021}). The pattern of flowering and fruiting is in agreement with the expectations and reflects the behavior of the reproductive phenology of the complete tree flora of the ECLJ. The reasons for this pattern would be the same as those previously indicated for all the tree species in the area.

Relative humidity and precipitation were the two environmental factors with the greatest influence on flowering, which appears to decrease in response to them (Table 2). The explanation for this is that these environmental factors exert an influence on both the flowers and the activity of pollinators (^{Janzen, 1967}). Higher humidity and water entail a greater difficulty for the activity of pollinators, whose mobility they hinder; the flowers also become less rewarding, as the nectar is diluted and its nutritional quality decreases; furthermore, the number of flowers is reduced due to the impact of the drops of water, which increase their weight; there is also more cloudiness and, consequently, the daylight hours are fewer, which reduces the pollinators’ activities (^{Janzen, 1967}).

The variables temperature, evaporation, and insolation do not seem to fluctuate much in the area, nor did not show a significant relationship with the richness of flowering, contrary to the evidence registered in other regions (^{Siegmund et al., 2016}) (Table 2).

The richness of fruiting species exhibited a clear tendency to decrease with increasing relative humidity (p≤0.0561) and with the increase in precipitation, as indicated by the literature (^{Cornejo and Ibarra, 2007}; ^{Cortés-Flores et al., 2012}); this tendency is attributed to the fact that the species maximize the time of moisture availability for the diaspores to germinate and for the seedling establishment to take place (^{Janzen, 1967}).

The richness of flowering and fruiting species was higher at an altitude range of 1 700 to 2 000 masl, with a very noticeable decrease above 2 100 m, due to an area effect, as 67 % of the surface area of the ECLJ is located within the altitudinal range of 1 700-2 000 masl, and <1 %, above 2 200 masl (Figure 6).

Conclusions

The flowering and fruiting patterns of the tree species in the study area coincide with those registered for dry tropical forests, humid forests with a certain degree of seasonality in precipitation, and humid temperate forests in Mexico, as well as in other regions of Central America.

The most important seasonal condition to which the reproductive phenology of the trees of the LJCS seems to respond is determined by relative humidity and precipitation; however, there are always species with flowers or fruit all year round.

In the study area, environmental factors such as temperature, insolation, and evaporation do not vary much throughout the year, and their effects on the reproductive phenology patterns of tree species do not seem to have much influence.

For a better understanding of the phenological patterns of plant species in the ECLJ, it is necessary to analyze the reproductive phenology of shrubs and herbaceous plants, including in the analysis the pollination and dispersal syndromes of the species.