Introduction

Swietenia humilis Zucc. it is a forest species of high ecological and socioeconomic importance that is distributed along the Pacific coast of Mexico and Central America (^{Rosas et al., 2011}). Its wood is of excellent quality and medicinal properties have been attributed to it, for which it has been the subject of pharmacological studies (^{Flores et al., 2019}). However, the distribution area and size of the natural populations of S. humilis have decreased rapidly (^{Rosas et al., 2011}). Due to the fragmentation of its habitat, it is common to find isolated trees or small remnant stands, which has affected its natural regeneration and genetic diversity (^{Rosas et al., 2011}). For example, in the Chamela-Cuixmala Biosphere Reserve, allelic richness in seeds from isolated populations was lower (6.1 alleles per locus) compared to that from continuous forests (8.3) (^{Rosas et al., 2011}). Consequently, S. humilis is included in the red list of threatened species of the International Union for Conservation of Nature (^{Barstow, 2019}).

The reduction and loss of natural populations of S. humilis justifies the need to implement actions for its conservation and sustainable use. For species under similar conditions, seed storage in germplasm banks, reforestation and restoration projects are the main ex situ and in situ conservation and preservation strategies that have contributed to the sustainability of such forest genetic resources (^{Ledig, 2004}). However, the limited availability of good quality germplasm, mainly from the genetic and physiological components, limits the success of these conservation, preservation and management strategies (^{Núñez-Cruz et al., 2018}).

The collection of germplasm of native species does not guarantee fruits and seeds with the sufficiency and quality required (^{Aitken, 2004}); the latter in terms of viability, vigor and germination capacity. This is explained because, for the most part, the material comes from small and fragmented populations or from isolated individuals, in which the parental sources suffered impacts at the genetic level (^{Pereira et al., 2020}). On the one hand, it is argued that these sources of germplasm are not the most appropriate due to the adverse effects caused by habitat fragmentation on the productivity and reproductive success of forest species (^{Broadhurst and Boshier, 2014}; ^{Melo et al., 2021}); on the other, it is emphasized that the use of local seed sources should be prioritized to meet the immediate demands for germplasm in reforestation and restoration programs on a small and medium scale (^{Melo et al., 2021}), since this genetic material is better adapted to the conditions of the plantation sites (^{Broadhurst and Boshier, 2014}).

A relevant guideline is to collect germplasm in local populations, specifically when it comes to native species whose biological and forestry knowledge is limited (^{Luna-Nieves et al., 2019}). However, it is important to know the characteristics such as the size of the fruits and the number of seeds they produce, as well as their weight and germination capacity, which is necessary information for good germplasm management and to better plan future breeding projects, conservation or propagation (^{Valverde-Rodríguez et al., 2019}).

There are few studies aimed at describing the fruits and seeds of S. humilis. Some antecedents are the works carried out by ^{Patiño (1996)} and ^{González-Vélez et al. (2020)}. It is necessary to generate information to identify local sources of good quality germplasm to meet the demands of germplasm banks and forest nurseries. The objective of this study was to analyze the morphometric and reproductive characteristics of S. humilis fruits in six sites in the state of Guerrero, as well as the viability and germination capacity of its seeds. It is hypothesized that there are differences in the morphometric and reproductive characteristics of S. humilis fruits, as well as the viability and germination capacity of its seeds among the six study sites.

Materials and Methods

The germplasm of S. humilis was collected in February 2020 in natural stands of six populations in the state of Guerrero, Mexico (Table 1).

Based upon the criteria for the identification and establishment of forest germplasm production units (^{Conafor, 2016}), five trees with outstanding phenotypic characteristics were selected at each site: clean stem (≥3 m) with straightness, larger crown according to visual inspection, abundant presence of fruit, visible absence of pests and diseases. The normal diameter of all individuals was recorded, this ranged between 38 and 60 cm. From each tree, at least two fruits were collected from the middle part of the crown, to avoid the dehiscence of the capsules (^{Sol et al., 2016}) and these were transported in jute sacks to later reduce their moisture content by exposing them to the sun inside paper bags for five days.

Results

Characteristics of the fruits

The morphometric and reproductive characteristics of the fruits of S. humilis differed between sites (P?λτ;0.0001; Figure 1). The fruits with the largest diameter were those from Santa Fe, with an average value of 99.03 mm, which was 56 % greater than the diameter of the fruits from Cieneguillas, which were the smallest (Figure 1a). For its part, Zacapalco presented the fruits with the longest length (15.27 cm), almost double the length of those from Cieneguillas (8.73 cm) (Figure 1b). The heaviest fruits were those of Arcelia with 498.96 g, whose weight was four times greater than that of the Cieneguillas fruits, which, as in the previous variables, had the lowest values (Figure 1c). Tuxpan had the fruits with the highest proportion of undeveloped seeds (39.23 %) (Figure 1d) although on average, it recorded the highest total number of seeds with around 70 per fruit (Figure 1e). In contrast, Cieneguillas presented a higher proportion of developed seeds compared to Tuxpan (Figure 1d), but presented the lowest number of seeds (64) per fruit (Figure 1e).

Bars represent means ± standard deviation. Means with a letter in common are not significantly different (P>0.05).

Figure 1 Morphometric and reproductive characteristics of Swietenia humilis fruits at six collection sites in Gurrero, Mexico.  

Unlike both sites, Santa Fe recorded the highest proportion of developed seeds (76.34 % of a total of 70) followed by Zacapalco, which also registered high values (76.06 % of a total of 70) in this variable (Figure 1d). The seeds developed from Zacapalco were the heaviest with an average weight per seed of 0.84 g, which is 140 % higher than the weight of 0.35 g recorded in Cieneguillas (Figure 1f). These differences in weight are also shown by the values for the weight of a thousand seeds and the number of seeds per kilogram, so that a thousand seeds from Zacapalco weigh almost 500 g more than those from Cieneguillas and less than half is required for one kilogram (Table 2).

Table 2 Weight of a thousand seeds and number of seeds per kilogram of Swietenia humilis Zucc. in each of the study sites. 

Collection site	Weight of 1 000 seeds (g)	Number of seeds per Kg
Zacapalco	839.7±154.9d	1 260.5±436.3a
Buenavista	537.5±67.8b	1 897.4±315.0c
Santa Fe	686.0±84.6cd	1 484.2±237.9ab
Cieneguillas	354.5±65.5a	2 926.3±606.3d
Tuxpan	688.9±130.4c	1 496.6±254.0b
Arcelia	572.3±137.1b	1 875.9±583.8c

Means ± standard deviation. Means with a letter in common are not significantly different (P>0.05).

Emergence

Emergence began 10 days after planting and the maximum accumulated emergence was obtained at 22 days (Figure 2). In the seeds of Zacapalco, Buenavista and Santa Fe, there was an emergency from day 10 and one day later an emergency was registered in the seeds of Cieneguillas, Arcelia and Tuxpan. Zacapalco registered the maximum accumulated emergency with 86 % and those of Arcelia the minimum, with only 17 % (Figure 2). Likewise, there were significant differences in the emergence parameters for all sites (P?λτ;0.0001; Figure 3).

Figure 2 Cumulative emergence curve of Swietenia humilis Zucc. seeds from six collection sites in the state of Guerrero, Mexico. 

Bars represent means ± standard deviation. Means with a letter in common are not significantly different (P>0.05).

Figure 3 Maximum emergence value (a), average daily emergence (b), germination value (c) and emergence percentage (d) in Swietenia humilis seeds from six collection sites in Guerrero, Mexico.  

According to the cumulative emergence trend, Zacapalco and Buenavista had the seed with the highest percentage of emergence, which was higher than 80 % (Figure 2). In turn, Zacapalco stood out with the highest observations in peak value, average daily emergence and germination value (3a, b and c). In contrast, the percentage of emergence of the seeds of the others was lower. Tuxpan, Cieneguillas and Santa Fe registered an emergence percentage that ranged between 80 % and 60 %, together with the respective reduction in the values of the germination parameters (Figure 3a, b, c and d). The Arcelia seed presented a drastic reduction in the values of all the emergency parameters (Figure 3), for example, when comparing their emergence values against those of Zacapalco, there is a difference of almost 70 % (Figure 3d).

Discussion

The variation in the size and weight of the fruit and the amount of seed produced recorded by S. humilis is a condition that has also been recorded in S. macrophylla King at the stand level (^{Pramono et al., 2019}) and families (^{Niembro and Ramírez -Garcia, 2006}); however, the average values in the size and weight of the fruits, as well as the amount of seeds contained in them, are similar to the values for S. humilis (^{Patiño, 1996}).

In Zacapalco, Santa Fe and Arcelia, the largest fruits (size and weight) and the heaviest seeds were found, a response that can be explained hypothetically with the reproductive effort of the trees (^{Turner, 2001}), which usually varies and is influenced by internal factors such as the reproductive success of each parental source as well as the availability of nutriments that affect seed development (^{Pramono et al., 2019}).

There is a close relationship between the size or weight of the seeds and the amount of reserves they contain (^{Kitajima, 2007}). These characteristics affect seedling growth rates and their competitive ability under natural conditions (^{Khurana and Singh, 2001}; ^{Kitajima, 2007}). In practice, the size of the seed is an important characteristic to produce plants in the nursery, since in some species such as Enterolobium contorsiliquum (Vell.) Morong (^{Trindade-Lessa et al., 2015}) and S. macrophylla (^{Pramono et al., 2019}), larger or heavier seeds tend to germinate faster and in a more uniform way.

The magnitude of the variation in the weight of the seeds recorded between the studied sites, based on the difference between the seeds of Zacapalco and those of Cieneguillas, can be attributed to the fact that the amount of reserves in the seeds that each tree produces depends, in turn, the number of fruits that it is able of producing, since a plant can invest both in a reduced number of larger or heavier seeds, as well as in more but smaller seeds (^{Kitajima, 2007}). However, to verify this assumption it is necessary that, in subsequent studies, the total production of fruits is also counted because in this study it was not planned to assess that aspect.

On the other hand, although it has been reported that in the morphology of the fruits there are traits that remain constant within the same species, such as the size of the fruit and its number of seeds (^{Sol et al., 2016}), the actual data indicate differences in these characteristics between the evaluated sites. Additionally, this last author also mentioned that there are other traits that are not kept constant and that exhibit variations between and within the parental sources, such as germination capacity and seed vigor. This is corroborated by the results of the germinative parameters obtained in this study. This behavior is explained by the wide variation in the germination response recorded by some forest species, such as Enterolobium cyclocarpum (Jacq.) Griseb., depending on the origin of the material due to the influence of environmental conditions such as temperature, humidity, light and soil fertility (^{Viveros-Viveros et al., 2017}).

In the germinative response, the seed from Zacapalco and Buenavista are outstanding, so that these sites may have potential as local sources of germplasm in the study region. This condition is supported by the data reported with S. humilis seeds collected in Huehuetlán el Chico municipality, Puebla State (^{González-Vélez et al., 2020}), because the figures recorded in germination coincide with the values determined in recently collected seeds in that area. It should be noted that for the differences in emergence, the influence of the genetic quality of each parental source is not excluded, mainly because S. humilis is a threatened species by the fragmentation of its habitat, and a consequence of the fragmentation of the natural populations so documented, is precisely the affectation of the germinative capacity (^{Pereira et al., 2020}).

In addition, the high proportion of undeveloped seeds recorded in Tuxpan or the limited germination capacity of the sites with germination percentages below 70 %, may be evidence of a decrease in the reproductive success of S. humilis due to negative impacts on the genetic diversity as argued by ^{Broadhurst and Boshier (2014)}, and experimentally demonstrated by ^{Rosas et al. (2011)} with populations of S. humilis from the Pacific coast in the state of Jalisco.

However, given that the other sites, mainly Zacapalco and Santa Fe, had fruits with high production of developed seeds and high germination capacity, it is recommended that the hypothesis of the effect on reproductive capacity be verified with studies at the genetic level with an experimental approach similar to that of the studies by ^{White et al. (2002)}, ^{Moraes et al. (2018)}, ^{Garcia et al. (2019)} and ^{Manoel et al. (2021)} because, in addition, in several tropical species a reduction in their genetic diversity has not been observed despite suffering fragmentation in their natural populations.

This is particularly true for S. humilis. A study carried out in fragmented natural populations in regions of Central America, confirms that the remnant patches of trees and isolated individuals have an important role in maintaining genetic connectivity and improving the variability of populations because they buffer the deleterious genetic effects of habitat destruction (^{White et al., 2002}). These implications are supported by the fact that S. humilis and its congener S. macrophylla are predominantly allogamous species that preserve high levels of diversity and genetic connectivity, thanks to their cross-mating system due to a certain degree of self-incompatibility and dichogamy, as well as their generalist pollination system and long-distance dispersal (^{White et al., 2002}; ^{Lemes et al., 2007}).

Finally, the results of this study also suggest how decisive the collection date is in the quality of the germplasm, based on the notoriety of the germinative responses of the Arcelia seeds, which in this case were the worst. Although the trees at this site produced large fruits with enough seeds of an intermediate weight, it is possible that the date of collection there was not appropriate, because the seeds of some fruits did not have the characteristic brown hue with which they are grown in the fieldand that it can visually define its maturity (^{Salazar et al., 2000}). Several studies with forest species from the tropics have emphasized the importance of defining adequate harvesting times due to the asynchrony in maturity that the species have at the tree or population level according to their distribution interval (^{Núñez-Cruz et al., 2018}; ^{Luna-Nieves et al., 2019}). This is particularly important for native tropical species such as S. humilis, because information on reproductive phenology is lacking for several local populations, such as that already generated for other species of the dry tropics (^{Núñez-Cruz et al., 2018}).

Conclusions

The S. humilis trees from the natural stands analyzed in the state of Guerrero, produce fruits and seeds that differ in their morphometric and reproductive characteristics, as well as in their germination capacity. This information has important implications because it serves as the basis for defining their use as local sources of germplasm to meet the demands for this small or medium-scale material for conservation, propagation and reforestation initiatives that are promoted with the species.