The broad cultivation of non-local species in urban areas or their introduction in natural vegetation, regardless of their origin, may offer a potential risk to local species in many aspects, as affecting the niches and interaction networks [1] [2] [3] . They are commonly called invasive or alien species. In this context, the biology of alien species received attention in recent studies [3] . Some seed germination features have been related to the invasive ability in many alien species and were evaluated in some places in Europe [4] , but there are no similar studies, as far as we know, regarding Neotropical plants.

Studies in the last two decades about seed germination patterns of Cerrado species [5] may allow some initial comparisons. Some differences in seed ecology between alien or invasive and local or native species were identified focusing on germinability, different light conditions for germination, stratification requirements, dormancy strategies, seedling growth or vigour and other traits [6] [7] [8] [9] [10] .

Tropical Malvaceae-Bombacoideae and Melastomataceae trees are widely cultivated around the world and some species of these groups present an invasive potential. Melastomataceae is a highly diverse worldwide family, with ca. 4500 species according to Clausing & Renner [11] , and some species show a high invasion potential around the world. The most famous invasive species are Clidemia hirta D. Don [12] and Miconia calvescens DC. [13] , but the list is increasing with Heterotis rotundifolia (Sm.) Jacq.-Fél., which has been considered invasive in many countries [14] . Recently, species from the Atlantic Forest as Tibouchina granulosa (Desr.) Cogn. and T. pulchra Cogn. [15] are being widely cultivated in urban areas of the Cerrado domain and also show some invasive potential. Tibouchina granulosa and T. pulchra are not viewed as alien or invasive species, but their cultivation may represent threats to local species. They usually occur as native species in the Atlantic Forest, but their habit and exuberant flowering has stimulated their cultivation in Brazilian urban areas [16] .

Special attention should be given to Heterotis rotundifolia, originated in African savannas [17] , which occurs from forests to open areas, roadsides and disturbed areas, because it is a fast-growing species, and due to its decumbent herbaceous habit that forms dense mats, it could displace natural vegetation [18] [19] . Although it has viable seeds, this species has vegetative growth and reproduction and, for this reason, it was included in the Global Compendium of Weeds [14] , and was listed as invasive and a weed species around the world [19] [20] [21] [22] . H. rotundifolia in Brazil was introduced in urban areas for cultivation, mainly for its dense mats and attractive flowers. Its present distribution in Brazil is sub-estimated due to the low number of surveys in urban areas, especially for non-arboreal plants, but it occurs in the states of Minas Gerais and Amazonas [23] .

In Bombacoideae (Malvaceae), some species also have a strong potential for cultivation in urban areas, especially due to their flowering and human seed consumption. Two of these species are cosmopolitan trees and cultivated around the world, Bombax ceiba, originated from Asia, and Pachira glabra, which has an uncertain origin. Robyns [24] suggests that P. glabra has its origin in the Tropical American Forests, with occasional and non-natural occurrence in disturbed and human altered areas of Cerrado. Pachira glabra is an alien in Cerrado areas, but it is commonly cultivated in urban areas inside the Cerrado Biome [25] .

This paper wants to describe the seed germination or seedling emergence pattern of five species of Bombacoideae and Melastomataceae commonly cultivated in urban areas surrounded by Cerrado, comparing them to local species from the same family and local flora.

The alien Bombacoideae species showed similar seed germination and seedling emergence pattern in relation to native Cerrado species of the same family, with high germinability and percentage of emergence, low germination or emergence time and synchronous processes [5] [37] [38] . Low germinability and percentage of emergence, with high germination or emergence time and asynchronous germination observed for seeds (or seedlings) of other Malvaceae tribes are associated with seed dormancy [5] [39] . It is very important to observe some attributes of seeds during the germination or emergence process to consider dormancy, that is, the quantity activated that is expressed by embryo protrusion or seedling emergence through time. This is the velocity of the process, which is measured by means of distribution over time. Dormancy can also be measured by synchrony. Dormant seeds, in general, show low velocity of embryo protrusion or seedling emergence and asynchrony, spreading the process through time. In reality, more important than the mean germination/emergency time is the amplitude between the first and last event, as was demonstrated for diaspores of Lithraea molleoides (Vell.) Eng. [43] . The total seeds germinated or seedlings emerged frequently are more associated with viability than with dormancy.

For Melastomataceae, we found some differences. The seed germination pattern of Heterotis rotundifolia was similar to Clidemia hirta. The latter is considered an invasive species [12] , with high germinability, slow and asynchronous seed germination [44] . Seeds of both species are probably dormant, but the type of dormancy is unknown. The dormancy types and metabolism in Melastomataceae are poorly known, although some studies have showed multiple dormancy [36] , physiological dormancy [45] and water impermeability in seed coat [46] . The spreading of the germination through time, typical of seeds of several Melastomataceae, permits the inclusion of these seeds in the category of relative dormancy as proposed by Labouriau [47] , but the type of dormancy is unclear because the spreading of the germination through time can be due to physical, morphological, physiological or combination of these causes. Dormancy is also present in other invasive species [6] [8] [9] , reinforcing the risk related to the cultivation of Heterotis rotundifolia near natural areas.

The germination process for Melastomataceae species usually starts in less than 30 days and is associated with dormancy in many species [41] [44] because more important than this limit, as was proposed by Baskin and Baskin [48] to consider seeds non-dormant, is the behaviour of the germination process through time. The spreading of the germination through time, that is, the broad range between the first and last germination or emergence is the most important reference point to consider dormancy and it is valid for species of other families. For example, seeds of Luehea divaricata, Ormosia arborea and Virola sebifera with dormancy, had a mean germination time of 24.1, 25.7 and 24 days, respectively, but with a range of the germination process from 4 to 104, 8 to 86, and 16 to 44 days, respectively [5] . The same species had a mean emergence time of 62.8, 80.4 and 57.7 days and a range of the emergence process from 29 to 105, 57 to 145 and 46 to 66 days, respectively. During this time, they reached 48.1%, 96% and 96% of germinability and 53, 89 and 15.7 of emergence. Seedlings of Copaifera langsdorffii and Genipa americana reached 95% and 84.5% of emergence with mean a emergence time of 27 and 28.7 days, ranging from 18 to 56 and 17 to 71 days [5] . All of them had the mean germination or emergence time lower than 30 days and relative dormancy due to the spreading of germination or emergence through time. Seeds of Luehea divaricata have relative dormancy caused by physiological dormancy, of Ormosia arborea have physical and mechanical dormancy, of Virola sebifera have physiological dormancy, and those of Copaifera langsdorffii have physical, chemical and physiological dormancy (see the relative frequency of germination or emergence in Ranal et al. [5] and more information for C. langsdorffii in Pereira et al. [49] . It is also important to consider that the low mean germination time of some species is associated with time censoring of the experiment, a particular decision of the researcher but, in these cases, the time measurements are underestimated. Another point is that for some species with dormant seeds that show a broad range between the first and last germination and very low synchrony, as is the case of Enterolobium contortisiliquum, Guazuma ulmifolia, Hymenaea courbaril [5] , Lithraea molleoides [43] , Senna sylvestris and Trema micrantha [5] , the mean germination time does not have the same importance or utility as for those that germinate very closely, even if this occurs after a long time. The relative frequency of germination or emergence and the survival analysis seems to be more appropriate for these species as pointed out by Berger et al. [43] . The last point is that seeds of some species could take a long time for the first germination, but most of them could germinate synchronously a long time after they were sowed. The seeds were dormant and this condition could be broken at the same time, weeks or months after sowing.

Regardless of the question of criterion, seeds of the Melastomataceae species, for example, specifically for Cerrado, show mean germination time values below 30 days [36] [41] [44] [45] [50] [51] [52] , reinforcing the importance of the high mean germination time and germination time of the last seed values found here for H. rotundifolia seeds.

The spreading of germination through time is associated with dormancy and this character permits soil seed bank formation for Melastomataceae, as was observed for Clidemia hirta, Miconia chartaceae, Miconia ferruginata, Microlicia fasciculata [36] [41] [44] [45] [53] [54] and Miconia ferruginata (MA Ranal, personal observation). Seeds of Clidemia hirta when unearthed, show a faster and synchronic germination process than seeds stored in paper bags in laboratory conditions [44] , and these results represent irrefutable evidence of its ability to survive in soil and form soil seed banks. Thus, this behaviour is an important signal that seeds of Heterotis rotundifolia can persist in seed banks, and in favourable situations can compete with the natural vegetation, although this character needs to be investigated. Seeds of Miconia albicans established in grasslands have slow and asynchronous germination, and this fact could increase seedling survival in grasslands, a more unpredictable environment compared to woodlands [52] .

Another important factor for the establishment of invasive species is that a larger introduction is more important to survival than small and frequent insertions [10] . Heterotis rotundifolia could incorporate the two processes with multiple insertions, one of them by means of the relative dormancy of its seeds that spread the germination through time, which represents the small and frequent insertions, and a second type represented by large introductions due to the high germinability of the seeds present in the soil seed banks, when exposed to ideal conditions for germination. It was observed for Leucaena leucocephala (Lam.) de Wit, another invasive species of the Cerrado region, that it also has its invasive capacity related to seed bank formation due to dormancy and high seed production [9] .

The low germinability of Tibouchina pulchra and T. granulosa seeds is comparable to seeds of Miconia ferruginata [44] and Microlicia fasciculata [41] . Miconia ferruginata presents high embryoless seed percentages [44] , a fact that could be present in the seeds of the two Tibouchina species. Studies have demonstrated that germinability of 27.84% and 23.92%, respectively for seeds of Tibouchina pulchra and T. granulosa [55] is related to the absence of embryos in their seeds, a common character in Melastomataceae [56] .

For Tibouchina pulchra and T. granulosa, low germinability could also represent reproductive inadequacies for local conditions, for example, soil quality. The urban area that was studied here has a high plant and animal diversity, and probably has no deficiency in pollination services. As the seed quality and germination pattern in some Cerrado Melastomataceae could be also related to aluminium presence [41] [44] , the presence of this element in Cerrado soils could be a disadvantage to non-Cerrado species as Tibouchina pulchra and T. granulosa. Heterotis rotundifolia might not be affected by this element taking into account its origin in African savannas, with possibly similar soil conditions. The last important point for some invasive species is that a low germination percentage has been found and that is compensated with other features as seedling vigour [6] .

Heterotis rotundifolia represents high potential risks to local species, especially because of the high germinability and spreading of germination through time with a not yet known dormancy mechanism. Allied to these factors, this species shows fast growth and vegetative propagation [18] [19] . Thus, special attention is necessary in monitoring the spread of this species and the possible impacts in the local species of Cerrado.

Other seed germination characters have also been related to the success of alien species. We have the examples of Clausena excavata Burm., which germinates in broad light conditions [7] , Impatiens glandulifera Royle, which requires a short period of time for seed stratification [6] , and alien Impatiens species, which have a more successful local adaptation rate compared to local Impatiens species [8] .

Besides this information, seed germination characters are not generally related to the capacity of invasion, except high germination rates [57] , probably because of the low number of comparative studies for other metrics related to seed germination. Another point is the absence of studies that compare seed germination patterns of species when they are in their native area and when they are alien. Unfortunately, we do not know the seed germination measurements for the alien species studied here in their natural habitat.

Our data could present some limitations due to the low number of trees evaluated, statistical inference and low number of species and families studied, but they represent the first data for some species, regardless of being in natural or alien areas. These descriptive data could improve information to plan future experimental investigations.

In conclusion, our data show two possible different patterns. Bombacoideae alien species studied here show the same seed pattern of local species, without a distinctive factor in seed germination or seedling emergence. On the other hand, Melastomataceae shows one species with a distinct pattern, Heterotis rotundifolia, which could offer risks to local flora. This species had a similar behaviour of other dormant species of the Cerrado flora.

Although we did not evaluate the entire process of the introduction of alien or cultivated species, the analyses of seed germination and seedling emergence measurements, as the spreading of germination in time, could offer information that is related to the success of invasive species.

We would like to thank the Universidade Federal de Uberlândia; all authors that released the data and Roger Hutchings for the English review. This work was funded by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior, Conselho Nacional de Desenvolvimento Científico e Tecnológico and Fundação de Amparo à Pesquisa do Estado de Minas Gerais. Some data of this study are part of the Doctoral thesis of the first author in the Programa de Pós-graduação em Ecologia e Conservação de Recursos Naturais.

The authors declare no conflicts of interest regarding the publication of this paper.

Mendes-Rodrigues, C., Oliveira, P.E., Marinho, R.C., Romero, R. and Ranal, M.A. (2019) Are the Alien Species of Melastomataceae and Bombacoideae a Potential Risk for Brazilian Cerrado? Open Access Library Journal, 6: e5156. https://doi.org/10.4236/oalib.1105156