140 RBCIAMB | n.49 | set 2018 | 140-150 Mateus Henrique Freire Farias Biology undergraduate student at Federal University of Piauí (UFPI) - Teresina (PI), Brazil. André Bastos da Silva MSc. in Development and Environment at the UFPI. PhD. student in Development and Environment at UFPI – Teresina (PI), Brazil. Aníbal Silva Cantalice Graduate in Biology at the UFPI. MSc. student in Development and Environment at the UFPI – Teresina (PI), Brazil. Maria Jaislanny Lacerda e Medeiros PhD. in Vegetal Biology at the Federal University of Pernambuco (UFPE). Professor of the Graduation’s degree in Field Education (UFPI) – Teresina (PI), Brazil. Clarissa Gomes Reis Lopes PhD. in Botany at the Federal University of Pernambuco (UFRPE). Professor of the Graduate Program in Development and Environment at the UFPI – Teresina (PI), Brazil. Corresponding address: Clarissa Gomes Reis Lopes – Universidade Federal do Piauí, Campus Ministro Petrônio Portella, Licenciatura em Ciências da Natureza – Avenida Universitária, s/n – Ininga – CEP 64049-550 – Teresina (PI), Brazil – E-mail: clarissa@ufpi.edu.br Received on: 08/07/2018 Accepted on: 11/17/2018 ABSTRACT Urbanization can alter environmental factors that affect the morphological and germinative characteristics of seeds. We evaluated the influence of an urban-rural gradient on the morphometrics of the fruits and seeds of Cenostigma macrophyllum Tul. (Fabaceae) and on seed germinability in the region near Teresina, Piaui State, Brazil. One hundred fruits were collected in the urban zone and 100 in the rural area, and the lengths, widths, thicknesses, and weights of both the fruits and seeds were measured, as well as the numbers of seeds per fruit. The seeds were then used in greenhouse germination experiments (during two months) to calculate the percentages of emergence (E%) and survival (S%), the emergence rate index (ERI), synchronization index (Z), and Timson’s index (T). The results showed significant statistical differences between the two areas in terms of the biometric patterns of the fruits and seeds as well as seed germination, with higher values in the urban zone. As such, urbanization was found to affect the morphologies and germination processes of plant species. Keywords: ecophysiology; semideciduous seasonal forests; caneleiro. RESUMO A urbanização altera os fatores ambientais, que podem afetar as características morfológicas e germinativas das sementes. Dessa forma, objetivou-se avaliar a influência do gradiente urbano-rural sobre a morfometria de frutos e sementes e germinabilidade de sementes de Cenostigma macrophyllum Tul. (Fabaceae) na região de Teresina, Piauí. Foram coletados 100 frutos na zona urbana e 100 na rural, sendo mensurados comprimento, largura, espessura, peso dos frutos e sementes e número de sementes por fruto. As sementes foram utilizadas no experimento de germinação em casa de vegetação, durante dois meses, sendo calculadas as porcentagens de emergência e de sobrevivência e mensurados os índices de velocidade de emergência, de sincronização e de Timson. Os resultados indicaram diferenças estatísticas entre as áreas para a biometria dos frutos e sementes e germinação de sementes, observando-se valores maiores para a zona urbana. Desse modo, foi possível concluir que a urbanização afeta a morfologia e o processo de germinação das espécies vegetais. Palavras-chave: ecofisiologia; floresta estacional semidecidual; caneleiro. DOI: 10.5327/Z2176-947820180369 MORPHOMETRIC STUDIES AND ANALYSES OF GERMINABILITY IN CENOSTIGMA MACROPHYLLUM TUL. IN AN URBAN-RURAL GRADIENT IN TERESINA-PI, BRAZIL ESTUDO MORFOMÉTRICO E ANÁLISE DA GERMINABILIDADE EM CENOSTIGMA MACROPHYLLUM TUL. NO GRADIENTE URBANO-RURAL EM TERESINA, PIAUÍ, BRASIL http://orcid.org/0000-0001-5901-2530 http://orcid.org/0000-0002-8414-6407 http://orcid.org/0000-0003-0205-5219 http://orcid.org/0000-0003-3912-5073 http://orcid.org/0000-0001-7290-4576 Morphometric studies and analyses of germinability in Cenostigma macrophyllum Tul. In an urban-rural gradient in Teresina-PI, Brazil 141 RBCIAMB | n.49 | set 2018 | 140-150 INTRODUCTION The lifecycles of plants include the critical phase of seed germination, which can directly influence their com- munity structure, species conservation, and forest re- generation (LIU et al., 2017; SOUZA; FAGUNDES, 2014). Germination processes vary between and within indi- viduals in many plant species (SEGURA et al., 2015) and are influenced by a wide set of factors, including seeds’ biological characteristics. The germination rate and seed germination speed of Artocarpus heterophyllus L. (Moraceae) in the tropical region of India, for exam- ple, were found to increase as a function of seed mass (KHAN, 2004). Other studies (e.g., SOUZA; FAGUNDES, 2014) have shown that seed weight and size are attri- butes can influence germination processes. Abiotic factors, such as temperature and water avail- ability, are among the environmental factors known to affect seed germination and seedling establishment (e.g., DOUSSEAU et al., 2013; MARAGHNI; GORAI; NEF- FATI, 2010), and temperature has been shown as hav- ing a strong influence on seed germination in humid and semiarid regions in Brazil (OLIVEIRA et al., 2013; ARAÚJO et al., 2016; RIBEIRO et al., 2015). The north- eastern region of that country includes extensive ar- eas of seasonally dry tropical forest (‘Caatinga’) whose plants are adapted to low rainfall levels (300–1,000 mm/year) (QUEIROZ et al., 2017) that affect seed ger- minability (FERREIRA; MEIADO; SIQUEIRA-FILHO, 2017; MEIADO et al., 2010). Investigations have shown that seed germination and seedling establishment can also be influenced by environmental variations provoked by anthropic actions, revealing potential threats to natu- ral ecological succession processes. Urban-rural gradients are among the anthropic phe- nomena that considerably alter many abiotic factors in the environment, such as temperature and humidity — which tend to be higher and lower, respectively, in urban areas as compared to rural sites (VALIN JR. et al., 2015). Those differences are related to the fact that urban areas have greater heat retention capacities (forming “Urban Heat Islands”) and demonstrate low humidity levels due to the greater impermeability of their soils and surfac- es (ARGÜESO et al., 2014). Those environments present the control of water availability by irrigation, with water availability being among the principal activators of the reproductive phase of plants – mainly in environments with well-defined dry seasons (ZHANG; ZHANG; TIAN, 2012). Those environmental factors observed in urban areas (and others, such as high CO2 levels and high so- lar radiation) can influence the morphological charac- teristics of fruits and seeds and, under favorable envi- ronmental conditions, it might be expected that their greater seed sizes and masses would positively influence germination and establishment. The western portion of the Brazilian semiarid region includes an extensive ecotone zone at the intersection of the Amazon Forest, Cerrado (Neotropical savanna), and Caatinga (deciduous, thorny, drylad vegetation) biomes and represents the largest phytoecological domain in the Parnaíba River Basin (PRB) (SOUSA et al., 2009). The climatic complexity and habitat heterogeneity found there, allied to the expanding urbanization (especially surrounding the principal urban centers) make the PRB region appropriate for studying the influence of urban- rural gradients on seed germination. Cenostigma macrophyllum Tul. (Fabaceae), popularly known as ‘caneleiro’, is widely distributed in the PRB (AGUIAR et al., 2016). That arboreal (or shrub) species is considered the plant symbol for the capital (Teresina) of Piauí State (Municipal Decree nº 2.407, August 13, 1993). In addition to having pharmaceutical properties (VIANA et al., 2013; COELHO et al., 2013), “caneleiro” is commonly used in arborization and landscaping proj- ects of urban areas (MACHADO et al., 2006). As such, the main objective of the present work was to evaluate the influence of the urban-rural gradient on the mor- phometrics of the fruits and seeds of C. macrophyllum Tul. (Fabaceae) and on seed germinability in the region near Teresina, Piaui State, Brazil. MATERIALS AND METHODS Study area The municipality of Teresina (4º47’25” – 5º35’11” S × 42º35’50” – 5º31’58” W) is situated in central-north- ern Piauí State, Brazil (IBGE, 2017). According to the Köppen classification system, the regional climate is Farias, M.H.F. et al. 142 RBCIAMB | n.49 | set 2018 | 140-150 hot and humid (Aw’) (JACOMINE et al., 1986), with a mean annual rainfall rate of 1393 mm, a mean annu- al temperature of 27.7ºC, and well-defined dry (June through October) and rainy (November through May) seasons (INMET, 2017). The region comprises a variety of phyto-ecological units, including semideciduous seasonal forests and Cerrado, and transition zones into forest and Caatinga areas (JACOMINE et al., 1986). C. macrophyllum is widely distributed throughout the region (QUEIROZ, 2009). The state capital of Teresina still retains some remnant forest areas, as well as many parks and squares with tree cover (MACHADO et al., 2006). Cenostigma macrophyllum individuals were selected for this study from both urban and rural areas: 1. along a tree-lined but heavily trafficked urban road (5º03’03”S × 42º44’19”W); 2. in a rural area near the BR-343 Highway (5º03’24”S x 42º41’W). Those “caneleiro” trees occurred in groups, without other nearby tree species. Data collection The experiments described here were undertaken at the Ethnobiology and Plant Ecology Laboratory (LEEV) and in greenhouses at the Federal University of Piauí (UFPI), between January and February/2017. We ran- domly collected 100 fruits of C. macrophyllum from both urban and rural areas (200 total mature fruits) to analyze their morphometrics. The lengths, widths, and thicknesses of the fruits were measured using digital calipers, with an accuracy of 0,01 mm; their masses were determined using a precision analytical balance, with accuracy of 0,0001 g. One hundred seeds from each area were randomly chosen for morphometric examination (measuring their lengths, widths, and weights as well as the num- bers of seeds per fruit) and subsequently used them in germination tests to determine any relationships between their morphometric values and germinability. The seeds were sown into trays containing topsoil, which were subsequently maintained in a greenhouse and watered daily. Each treatment consisted of four replicates of 25 seeds. Seedling emergence was eval- uated daily, adopting a definition of germination as the appearance of the seedling’s aerial portion on the substrate surface. The observations on germination continued for two months, ended by the absence of any seedling emergence during 10 consecutive days. We calculated the percentages of emergence (E%) and survival (S%) , obtained by the number of plants that emerged and survived by the number of the seeds used, respectively, the emergence rate index (ERI) was determined by the sum of plants that emerged on the day of the emergency (MAGUIRE, 1962). The synchronization index (Z) to verify the distribution of the relative frequency of germination during the study period, and Timson’s index (T), which represents the progressive total of the cumulative percentage of ger- mination recorded at specific intervals (each day of study) or a given period of time, higher values cor- respond to the better conditions of germination (RANAL; SANTANA, 2006). Statistical analyses Data’s normality and homoscedasticity were tested to calculate any differences between the morphomet- ric variables analyzed, using ANOVA and the Tukey a posteriori test. The widths did not demonstrate nor- mality, requiring the use of the Mann-Whitney test. The original data of the total weights of the seeds in each fruit did not demonstrate homoscedasticity and were square root transformed. Thickness data was x**1.5 transformed due to the observed high coefficient of variation (CV). The germination tests were entirely randomized and their data submitted to Generalized Linear Model (GLM) procedures to evaluate any differences between the two areas. Only seeds from the urban area were used to determine if seeds’ weights and sizes influ- enced their germinability, as the germination rates of seeds from the rural area were too low for accurate statistical analyses. GLM was used to compare the weights and sizes of the urban area’s germinated and non-germinated seeds, and the Spearman correlation Morphometric studies and analyses of germinability in Cenostigma macrophyllum Tul. In an urban-rural gradient in Teresina-PI, Brazil 143 RBCIAMB | n.49 | set 2018 | 140-150 test to examine any relationships between the num- bers of days required for germination and seed weights and sizes. All of the analyses were performed using SAS System 9.0 software. RESULTS AND DISCUSSION Evaluations of the Cenostigma macrophyllum fruits’ morphometric data revealed that the biometric means of the fruits harvested from the urban area were sig- nificantly greater than those harvested from the rural area, except for width (Table 1). The fruits from the urban area had: widths between 1.66 and 3.41 cm; thickness between 0.40 and 0.86 cm; lengths between 4.50 and 10.33 cm; weights between 2.90 and 12.85 g. Fruits harvested from the rural area had: widths be- tween 2.09 and 3.77 cm; thicknesses between 0.2 and 0.8 cm; lengths between 2.98 and 10.11 cm; and mass- es between 2.09 and 9.43 g. The morphometrics of the seeds were similar to those of the fruits, with their measurements being greater in the urban area when compared to the rural area (Table 1). The variable of width demonstrated the greatest numbers of seeds in the interval between 1.22 and 1.42 cm in the urban area, while the great- est numbers of seeds in the rural area were observed in the interval between 0.82 and 1.22 cm (Figure 1A). Large differences in seed thicknesses were observed between the two areas. The greatest numbers of seeds collected in the urban area were observed in the width interval between 0.243 and 0.390 cm; the seeds from the rural area were thinner, with the highest numbers within the width intervals from 0.094 to 0.243 cm (Figure 1B). In terms of seed length, most of the seeds collected in the urban area were in the length class 1.56 to 2.02 cm; while seeds from the rural area were largely included between the length interval of 1.33 to 1.79 cm (Figure 1C). The greatest numbers of seeds collected in the ur- ban area weighed between 0.292 and 0.584 g; while seeds from the rural area were largely included with- in the weight interval of 0.000 to 0.292 g. The seeds from the urban area were therefore both larger and heavier (Figure 1D), which most likely contributed to their higher germination rates (Table 2). Each fruit in the urban area contained from one to five seeds, with most having between one and four seeds; fruits from the rural area had from zero to four seeds, with most of them having either one or two seeds (Figure 1E). Table 1 – Mean values of the morphometrics of the fruits and seeds of Cenostigma macrophyllum Tul. harvested in urban and rural areas in the municipality of Teresina (PI), Brazil. Variables Urban area Rural area p* Fruit morphometry Width (cm) 2.74 2.84 p < 0.05 Thickness (cm) 0.65 0.45 p < 0.01 Length (cm) 7.48 7.32 n.s Fruit weight (cm) 6.66 5.26 p < 0.01 Number of seeds per fruit 2.19 1.32 p < 0.01 Weight of seeds per fruit (g) 1.03 0.27 p < 0.01 Seed morphometry Weight (g) 0.45 0.20 p < 0.01 Width (cm) 1.27 1.06 p < 0.01 Thickness (cm) 0.31 0.15 p < 0.01 Lenght (cm) 1.73 1.60 p < 0.01 p*: probability of significance. Farias, M.H.F. et al. 144 RBCIAMB | n.49 | set 2018 | 140-150 C. macrophyllum demonstrates phenotypic plastici- ty (a common capability among forest species), with wide morphometric variations being observed in their fruits and seeds (CRUZ; CARVALHO, 2003) due to endogenous factors, such as genetic variability (KRISHNAN; BORGES, 2018), and exogenous factors Figure 1 – Biometrics of the seeds of Cenostigma macrophyllum Tul. (A, B, C and D) and the numbers of seeds per fruit (E) harvested in urban and rural areas in the municipality of Teresina (PI), Brazil. Se ed s (n o ) Se ed s (n o ) Seeds (no) Fr ui ts (n o ) Se ed s (n o ) Se ed s (n o ) Width (cm) A 60 50 40 30 20 10 0 0.62 |- 0.82 0.82 |- 1.02 1.02 |- 1.22 1.22 |- 1.42 1.42 |- 1.62 1.10 |- 1.33 1.33 |- 1.56 1.56 |- 1.79 1.79 |- 2.02 2.02 |- 2.25 0.020 |- 0.094 0.094 |- 0.168 0.168 |- 0.243 0.243 |- 0.317 0.317 |- 0.390 0.000 |- 0.146 0.146 |- 0.2920 0.292 |- 0.438 0.438 |- 0.584 0.584 |- 0.730 60 50 40 30 20 10 0 60 50 40 30 20 10 0 1 2 3 4 5 6 60 Rural Urban 50 40 30 20 10 0 60 50 40 30 20 10 0 C E B D Thickness (cm) Length (cm) Weight (g) Morphometric studies and analyses of germinability in Cenostigma macrophyllum Tul. In an urban-rural gradient in Teresina-PI, Brazil 145 RBCIAMB | n.49 | set 2018 | 140-150 such as the availability of light, nutrients and water that can influence phenotypic variation (SILVA et al., 2012) and cause morphological alterations (MISHRA et al., 2014). Martins et al. (2005) examined the influence of seed weight on germination and seedling vigor in Carica papaya L. (papaya), and likewise reported that the heaviest seeds demonstrated the highest germination rates. Those results were like ours in the present work, as seeds collected in the urban area were heavier and demonstrated greater germination rates than the light- er seeds produced in rural areas, most likely reflect- ing the fact that larger seeds have more nutrient re- serves and greater advantages in terms of germination (ZHANG et al., 2016). In comparing the sizes and weights of germinated and ungerminated seeds from the urban area, it was observed that germinated seeds were significantly thicker than those that had not germinated; the oth- er morphometric characteristics examined here did not demonstrate any significant differences (Table 3). Only seed thickness was weakly correlated with the timing of germination, with thicker seeds germinating slightly quickly (R = 0.20; p < 0.05). These results indicated that their greater thickness was related to greater amounts of stored humidity or larger nutrient reserves. Silva and Carvalho (2008) observed that increases in the sizes of Clitoria fair- childiana R.A. Howard. (Fabaceae) seeds were not related to their water contents, supporting the idea that greater thickness is most likely related to their greater nutrient content. The C. fairchildiana seeds had all been collected in the same area, and prob- ably had similar water contents proportional to soil humidity. In the present study, the C. macrophyllum Tul. (Fabaceae) trees in the urban area were irrigated daily, which would presumably increase seed humidi- ty and, consequently, their thickness. Our results corroborated the published results relating to seed morphometrics and germination, which have shown that seed sizes and weights influence not only germination but also initial seedling development (BOUCHARDET et al., 2015), and that seed biometric measurements are directly related to their physiological quality and germinative viability (OLIVEIRA-BENTO et al., 2013). Seed germination indices in the two areas were sig- nificantly different, with greater percentages of plants Table 2 – Mean values of the germination of Cenostigma macrophyllum Tul. seeds in urban and rural areas in the municipality of Teresina (PI), Brazil. Parameters Urban area Rural area p* E% 55.00 4.00 0.02 S% 52.00 3.00 0.02 ERI 1.53 0.10 0.02 Z 2.30 0.50 0.02 T 5519.53 398.43 0.02 E%: Emergence percentage; S%: survival percentage; ERI: emergence rate index; Z: synchronization index; T: Timson’s index; p*: probability of significance. Table 3 – Mean sizes and masses of the germinated and non-germinated seeds of Cenostigma macrophyllum Tul. from an urban area in the municipality of Teresina (PI), Brazil. Variables Germinated seeds Non-germinated seeds p* Weight (g) 0.47 0.43 0.14 Width (cm) 1.27 1.26 0.98 Thickness (cm) 0.32 0.30 0.04 Lenght(cm) 1.72 1.71 0.87 p*: probability of significance. Farias, M.H.F. et al. 146 RBCIAMB | n.49 | set 2018 | 140-150 emergence and survival among those harvested from the urban area (Table 2). The emergence velocities of seeds harvested from the urban area were significantly higher than those from the rural area, both in terms of the partial numbers of germinated seeds (ERI) and the partial percentages of germination — using Timson’s index (T) for more precise comparisons. Greater ERI values directly influence a species’ emer- gence (E%) and survival percentage (S%), favoring a faster establishment and diminishing the chances seeds infection by pathogenic microorganisms or con- sumption by predators (FAGUNDES; CAMARGOS; COS- TA, 2011) — creating an evident relationship between greater emergence velocity and greater emergence and survival percentages. Carvalho and Nakagawa (2000) found that vigorous seeds with higher emergence capacities demonstrated high emergence velocities — while the opposite was observed with less vigorous seeds more susceptible to deterioration. Emergence percentage is also directly related to percentage survival, as greater numbers of germinating seeds indicate a greater probability of sur- vival (ZHANG et al., 2016). The synchronization index (Z) (which was greater for seeds harvested in the urban area) is of great im- portance to successful plant and plant community development as synchronous seed germination will tend to increase synchrony in all subsequent life cycle phases, including reproductive phenophases, with community synchrony being of extreme im- portance to efficient seed production and dispersal (MORELLATO et al., 2016). The high percentages of successfully germinating seeds collected from the urban area (and the probable rela- tionship with greater water availability in that environ- ment) demonstrates that C. macrophyllum seeds have a “hydric-memory”. Rito et al. (2009) observed that discontinuous cycles of hydration/dehydration favored the germination of Cereus jamacaru (Cactaceae) seeds, as a reflection of their hydric-memory, which appeared to preserve characteristics resulting from imbibition throughout the dry period, with germination only oc- curring when humidity conditions became favorable. Although the Cenostigma macrophyllum seeds used here were not exposed to cycles of hydration/dehydra- tion, it is possible that they had experienced contrasting situations of water availability in their development (due to fluctuations in soil water availability to the mother plant). The hydric-memory of a given species is reflected in its germinative behavior, which, in turn, is influenced by its surrounding environment, so that the urban-rural gradient may be affecting important eco-physiological characteristics that are important to the maintenance of species in their respective ecosystems. The importance of water availability for seed germi- nation has been discussed in the literature (PELEGRI- NI et al., 2013), and is considered one of the main factors gating their reproductive phase (NEIL et al., 2014) and a limiting factor for seed germination and seedling growth (DÜRR et al., 2015). Water availability represents one of the principal factors affecting fruit biometrics and the viability of C. macrophyllum seeds. Urbanization results in enormous environmental alteration (ARGÜESO et al., 2014) and is almost surely responsible for certain phenotypic variations in plants. The observed morphometric differences between fruits and seeds in the urban-rural gradient suggest that exogenous factors associated with urbanization are directly involved. Those factors can provoke changes in plant phenotypes as they adapt to urban environments, quite possibly making them less fit for establishment in natural environments and reducing their utility for restoration projects (BOTEZELLI; DAVIDE; MALAVASI, 2000). The different environments in urban and rural areas are known to act directly on the vegetative and reproduc- tive phases of plants (NEIL et al., 2014), so that their fruits’ morphological characteristics (as well as seed germination) will be affected by abiotic factors acting directly on plant structures. In addition to the availability of water resources, CO 2 assimilation can also alter the vegetative growth of plants and their biomass distributions (XU et al., 2014). Seed germination has been found to be strongly affected by atmospheric CO 2 levels and can cause allometric modifications of seedling growth (MARTY; BASSIRIRAD, 2014). As higher CO 2 concentrations will be found in urban areas, the resulting alterations in plant biomass allocation can result in the production of larger and better-quality fruits (AIDAR et al., 2002), as seen here with C. macrophyllum (except for seed width). Morphometric studies and analyses of germinability in Cenostigma macrophyllum Tul. In an urban-rural gradient in Teresina-PI, Brazil 147 RBCIAMB | n.49 | set 2018 | 140-150 REFERENCES AGUIAR, B. A. de S.; SOARES, E. S. S.; MASRUA, M. L. A.; OLIVEIRA, M. C. P.; LOPES, A. V. F.; SOUSA, G. M. Biologia floral e reprodutiva de Cenostigma macrophyllum Tul. (Fabaceae) no Parque Zoobotânico de Teresina, Piauí. Journal of Environmental Analysis and Progress, v. 1, n. 1, p. 84-95, 13 out. 2016. http://dx.doi.org/10.24221/jeap.1.1.2016.993.84-95 AIDAR, M. P. M.; MARTINEZ, C. A.; COSTA, A. C.; COSTA, P. M. F. I; DIETRICH, S. M. C. I; BUCKERIDGE, M. S. Effect of atmospheric CO2 enrichment on the establishment of seedlings of Jatobá, Hymenaea Courbaril L. (Leguminosae, Caesalpinioideae). Biota Neotropica, v. 2, n. 1, p. 1-10, 2002. http://dx.doi.org/10.1590/s1676-06032002000100008 ARAÚJO, A. M. S.; ASSIS, L. C. S. L. C.; NOGUEIRA, N. W.; FREITAS, R. M. O.; TORRES, S. B. Substrates and temperatures for the germination of seeds of Senegalia tenuifolia (L.) Britton & Rose. Revista Caatinga, v. 29, n. 1, p. 113-118, mar. 2016. http://dx.doi.org/10.1590/1983-21252016v29n113rc ARGÜESO, D.; EVANS, J. P.; FITA, L.; BORMANN, K. J. Temperature response to future urbanization and climate change. Climate Dynamics, v. 42, n. 7-8, p. 2183-2199, 5 maio 2014. http://dx.doi.org/10.1007/s00382-013-1789-6 BOTEZELLI, L.; DAVIDE, A. C.; MALAVASI, M. M. Características dos frutos e sementes de quatro procedências de Dipteryx alata vogel (baru). Cerne, Lavras, v. 6, n. 1, p. 9-18, 2000. BOUCHARDET, D. de A.; RIBEIRO, I. M.; SOUSA, N. A.; AIRES, S. S.; MIRANDA, H. S. Efeito de altas temperaturas na germinação de sementes de Plathymenia reticulata Benth. E Dalbergia miscolobium Benth. Revista Árvore, v. 39, n. 4, p. 697-705, ago. 2015. http://dx.doi.org/10.1590/0100-67622015000400012 CARVALHO, N. M.; NAKAGAWA, J. Sementes: ciência, tecnologia e produção. 4. ed. Jaboticabal: FUNEP, 2000. 588 p. COELHO, N. P. M. de F.; NOGUEIRA, V. C.; CARDOSO, M. A. G.; LOPES, L. S.; NASCIMENTO, P. P.; ROCHA, E. S.; SILVA, C. L. P.; ARISAWA, E. A. L. Cenostigma macrophyllum Tul. on the healing of skin wounds in rats with Diabetes mellitus. Acta Cirurgica Brasileira, v. 28, n. 8, p. 594-600, ago. 2013. http://dx.doi.org/10.1590/s0102-86502013000800007 CRUZ, E. D.; CARVALHO, J. E. U. de. Biometria de frutos e germinação de sementes de Couratari stellata A. C. Smith (Lecythidaceae). Acta Amazonica, v. 33, n. 3, p. 381-388, 2003. http://dx.doi.org/10.1590/s0044-59672003000300004 DOUSSEAU, S.; ALVARENGA, A. A.; ARANTES, L. O.; CHAVES, I. S.; AVELINO, E. V. Techonolgy of Qualea grandiflora Mart. (Vochysiaceae) seeds. Cerne, v. 19, n. 1, p. 93-101, mar. 2013. http://dx.doi.org/10.1590/s0104-77602013000100012 DÜRR, C.; DICKIE, J. B.; YANG, X.-Y.; PRITCHARD, H. W. Ranges of critical temperature and water potential values for the germination of species worldwide: Contribution to a seed trait database. Agricultural and Forest Meteorology, v. 200, n. 1, p. 222-232, jan. 2015. http://dx.doi.org/10.1016/j.agrformet.2014.09.024 CONCLUSIONS The fruits and seeds of Cenostigma macrophyllum Tul. (Fabaceae) collected in an urban area demonstrated biometric means and amplitudes larger than of those collected in a rural area; the germinabilities of seeds from the urban area were likewise significantly greater. These results indicate that abiotic factors within the ur- ban-rural gradient are acting directly on the growth and development of C. macrophyllum, the morphometrics of their fruits and seeds and seed germination. The data generated in the present study will be import- ant for better understanding the impacts of urbanization on natural ecosystems, and how abiotic factors along a rural/urban gradient directly affect plant growth and reproduction. Additional studies will still be needed; however, that can identify the environmental factors of urbanization that are directly affecting the reproductive fitness of those plants and the consequences of those alterations for the natural environment. Farias, M.H.F. et al. 148 RBCIAMB | n.49 | set 2018 | 140-150 FAGUNDES, M.; CAMARGOS, M. G.; COSTA, F. V. da. A qualidade do solo afeta a germinação das sementes e o desenvolvimento das plântulas de Dimorphandra mollis Benth. (Leguminosae: Mimosoideae). Acta Botanica Brasilica, v. 25, n. 4, p. 908-915, dez. 2011. http://dx.doi.org/10.1590/s0102-33062011000400018 FERREIRA, J. V. A.; MEIADO, M. V.; SIQUEIRA FILHO, J. A. de. Efeito dos Estresses Hídrico, Salino e Térmico na Germinação de Sementes de Handroanthus spongiosus (Rizzini) S. Grose (Bignoniaceae). Gaia Scientia, v. 11, n. 4, p. 57-64, 30 jul. 2017. http://dx.doi.org/10.22478/ufpb.1981-1268.2017v11n4.35470 INSTITUTO BRASILEIRO DE GEOGRAFIA E ESTATÍSTICA (IBGE). Teresina. IBGE, 2017. Disponível em: . Acesso em: 15 ago. 2017. INSTITUTO NACIONAL DE METEOROLOGIA (INMET). Dados históricos. INMET, 2017. Disponível em: . Acesso em: 18 maio 2017. JACOMINE, P. K. T.; CAVALCANTI, A. C.; PESSOA, S. P. C.; BURGOS, N.; MÉLO FILHO, H. F. R.; LOPES, O. F.; MEDEIROS, L. A. R. Levantamento exploratório de solos do estado do Piauí. In: EMPRESA BRASILEIRA DE PESQUISA AGROPECUÁRIA (EMBRAPA)-SERVIÇO NACIONAL DE LEVANTAMENTO E CONSERVAÇÃO DE SOLOS (SNLCS) (Org.). Boletim de pesquisa, v. 36, n. 18, p. 1-782, 1986. (Série Recursos de Solos). KHAN, M. l. Effects of seed mass on seedling success in Artocarpus heterophyllus L., a tropical tree species of north-east India. Acta Oecologica, v. 25, n. 1-2, p. 103-110, mar. 2004. http://dx.doi.org/10.1016/j.actao.2003.11.007 KRISHNAN, A.; BORGES, R. M. A fig tree in a concrete jungle: fine-scale population genetic structure of the cluster fig Ficus racemosa in an urban environment. Urban Ecosystems, v. 21, n. 1, p. 171-181, 2018. http://dx.doi.org/10.1007/ s11252-017-0707-9 LIU, X.; XU, D.; YANG, Z.; ZHANG, N. Geographic variations in seed germination of Dalbergia odorifera T. Chen in response to temperature. Industrial Crops and Products, v. 102, p. 45-50, ago. 2017. http://dx.doi.org/10.1016/j. indcrop.2017.03.027 MACHADO, R. R. B.; MEUNIER, I. M. J.; SILVA, J. A. A.; CASTRO, A. A. J. F. Árvores nativas para a arborização de Teresina, Piauí. Revista da Sociedade Brasileira de Arborização Urbana, v. 1, n. 1, p. 10-18, 2006. MAGUIRE, J. D. Speed of Germination—Aid In Selection And Evaluation for Seedling Emergence And Vigor. Crop Science, v. 2, n. 2, p. 176-177, 1962. http://dx.doi.org/10.2135/cropsci1962.0011183x000200020033x MARAGHNI, M.; GORAI, M.; NEFFATI, M. Seed germination at different temperatures and water stress levels, and seedling emergence from different depths of Ziziphus lotus. South African Journal of Botany, v. 76, n. 3, p. 453-459, ago. 2010. http://dx.doi.org/10.1016/j.sajb.2010.02.092 MARTINS, G. N.; SILVA, R. F.; ARAÚJO, E. F.; PEREIRA, M. G.; VIEIRA, H. D.; VIANA, A. P. Influência do tipo de fruto, peso específico das sementes e período de armazenamento na qualidade fisiológica de sementes de mamão do grupo formosa. Revista Brasileira de Sementes, v. 27, n. 2, p.12-17, dez. 2005. http://dx.doi.org/10.1590/s0101-31222005000200003 MARTY, C.; BASSIRIRAD, H. Seed germination and rising atmospheric CO2concentration: a meta-analysis of parental and direct effects. New Phytologist, v. 202, n. 2, p. 401-414, 24 jan. 2014. http://dx.doi.org/10.1111/nph.12691 MEIADO, M. V.; ALBUQUERQUE, L. S. C. ROCHA, E. A.; ROJAS-ARÉCHIGA, M.; LEAL, I. R. Seed germination responses of Cereus jamacaru DC. ssp. jamacaru (Cactaceae) to environmental factors. Plant Species Biology, v. 25, n. 2, p. 120-128, 21 abr. 2010. http://dx.doi.org/10.1111/j.1442-1984.2010.00274.x MISHRA, Y.; RAWAT, R.; RANA, P. K.; SONKAR, M. K.; MOHAMMAD, N. Effect of seed mass on emergence and seedling development in Pterocarpus marsupium Roxb. Journal of Forestry Research, v. 25, n. 2, p. 415-418, 30 abr. 2014. http:// dx.doi.org/10.1007/s11676-014-0469-7 Morphometric studies and analyses of germinability in Cenostigma macrophyllum Tul. In an urban-rural gradient in Teresina-PI, Brazil 149 RBCIAMB | n.49 | set 2018 | 140-150 MORELLATO, L. P. C.; ALBERTON, B.; CARSTENSEN, S. W.; ESCOBAR, D. F. E.; LEITE, P. T. P.; MENDONZA, I.; ROCHA, N. M. W. B.; SOARES, N. C.; SILVA, T. S. F.; STAGGEMEIER, V. G.; STREHER, A. S.; VARGAS, B. C.; PERES, C. A. Linking plant phenology to conservation biology. Biological Conservation, v. 195, p. 60-72, mar. 2016. http://dx.doi.org/10.1016/j.biocon.2015.12.033 NEIL, K.; WU, J.; BANG, C.; FAETH, S. Urbanization affects plant flowering phenology and pollinator community: effects of water availability and land cover. Ecological Processes, v. 3, p. 17, 22 ago. 2014. http://dx.doi.org/10.1186/s13717-014-0017-6 OLIVEIRA, A. K. M.; RIBEIRO, J. W. F.; PEREIRA, K. C. L.; SILVA, C. A. A. Effects of temperature on the germination of Diptychandra aurantiaca (Fabaceae) seeds. Acta Scientiarum. Agronomy, v. 35, n. 2, p. 203-208, 26 mar. 2013. http:// dx.doi.org/10.4025/actasciagron.v35i2.15977 OLIVEIRA-BENTO, S. R. S.; TORRES, S. B.; OLIVEIRA, F. N.; PAIVA, E. P.; BENTO, D. A. V. Biometria de frutos e sementes e germinação de Calotropis procera Aiton (Apocynaceae). Bioscience Journal, v. 29, n. 5, p. 1194-1205, 2013. PELEGRINI, L. L.; BORCIONI, E.; NOGUEIRA, A. C.; KOEHLER, H. S.; QUOIRIN, M. G. G. Efeito do estresse hídrico simulado com NaCl, manitol e PEG (6000) na germinação de sementes de Erythrina falcata Benth. Ciência Florestal, v. 23, n. 2, p. 511-519, 28 jun. 2013. http://dx.doi.org/10.5902/198050989295 QUEIROZ, L. P. Leguminosas da Caatinga. Feira de Santana: UEFS, 2009. 443 p. QUEIROZ, L.; CARDOSO, D.; FERNANDES, M. F.; MORO, M. F. Diversity and Evolution of Flowering Plants of the Caatinga Domain. In: SILVA, J. M. C. da; LEAL, I. R; TABARELLI, M. (Orgs.). Caatinga: The Largest Tropical Dry Forest Region in South America. Nova York: Springer, Cham, 2017. p. 23-63. RANAL, M. A.; SANTANA, D. G. de. How and why to measure the germination process? Revista Brasileira de Botânica, v. 29, n. 1, p. 1-11, mar. 2006. http://dx.doi.org/10.1590/s0100-84042006000100002 RIBEIRO, J. W. F.; OLIVEIRA, A. K. M.; RODRIGUES, A. P. D. C.; RONDON, E. V. Germination and morphology of seeds and seedlings of Parkia gigantocarpa Fabaceae: Mimosoideae. Floresta, v. 45, n. 2, p. 303-314, 5 mar. 2015. http://dx.doi. org/10.5380/rf.v45i2.34504 RITO, K. F.; ROCHA, E. A.; LEAL, I. R.; MEIADO, M. V. As sementes de mandacaru têm memória hídrica? Boletín de La Sociedad Latinoamericana y del Caribe de Cactáceas y Otras Suculentas, v. 6, n. 1, p. 26-31, jan. 2009. SEGURA, F.; VICENTE, M. J.; FRANCO, J. A.; MARTÍNEZ-SÁNCHEZ, J. J. Effects of maternal environmental factors on physical dormancy of Astragalus nitidiflorus seeds (Fabaceae), a critically endangered species of SE Spain. Flora - Morphology, Distribution, Functional Ecology of Plants, v. 216, p. 71-76, set. 2015. http://dx.doi.org/10.1016/j.flora.2015.09.001 SILVA, B. M. da S. e; CARVALHO, N. M. de. Efeitos do estresse hídrico sobre o desempenho germinativo da semente de faveira (Clitoria fairchildiana R.A. Howard. - Fabaceae) de diferentes tamanhos. Revista Brasileira de Sementes, v. 30, n. 1, p. 55-65, 2008. http://dx.doi.org/10.1590/s0101-31222008000100008 SILVA, C. B. da; LOPES, M. M.; MARCOS-FILHO, J.; VIEIRA, R. D. Automated system of seedling image analysis (SVIS) and electrical conductivity to assess sun hemp seed vigor. Revista Brasileira de Sementes, v. 34, n. 1, p. 55-60, 2012. http:// dx.doi.org/10.1590/s0101-31222012000100007 SOUSA, S. R.; CASTRO, A. A. J.; FARIAS, R. R. S.; SOUSA, G. M.; CASTRO, N. M. C. F. Fitoecologia do complexo de Campo Maior, Piauí, Brasil. Publicações Avulsas em Conservação de Ecossistemas, v. 22, p. 1-25, 2009. https://dx.doi. org/10.18029/1809-0109/pace.n22p1-22 SOUZA, M. L.; FAGUNDES, M. Seed Size as Key Factor in Germination and Seedling Development of Copaifera langsdorffii (Fabaceae). American Journal of Plant Sciences, v. 5, n. 17, p. 2566-2573, 2014. http://dx.doi.org/10.4236/ ajps.2014.517270 Farias, M.H.F. et al. 150 RBCIAMB | n.49 | set 2018 | 140-150 VALIN JUNIOR, M. de O.; RIBEIRO, K. A.; SANTOS, F. M. M.; NOGUEIRA, M. C. J. A.; MUSIS, C. R. Análise da variação higrotérmica entre área rural e urbana em período de nível crítico de umidade no Vale do Rio Cuiabá. Revista Eletrônica em Gestão, Educação e Tecnologia Ambiental, Santa Maria, v. 19, n. 2, p. 1392-1399, maio 2015. http://dx.doi. org/10.5902/2236117016864 VIANA, A. F. S. C.; FERNANDES, H. B.; SILVA, F. V.; OLIVEIRA, I. S.; FREITAS, F. F.; MACHADO, F. D.; COSTA, C. L.; ARCANJO, D. D.; CHAVES, M. H.; OLIVEIRA, F. A.; OLIVEIRA, R. C. Gastroprotective activity of Cenostigma macrophyllum Tul. var. acuminata Teles Freire leaves on experimental ulcer models. Journal of Ethnopharmacology, v. 150, n. 1, p. 316-323, out. 2013. XU, Z.; SHIMIZU, H.; ITO, S.; YAGASAKI, Y.; ZOU, C.; ZHOU, G.; ZHENG, Y. Effects of elevated CO2, warming and precipitation change on plant growth, photosynthesis and peroxidation in dominant species from North China grassland. Planta, v. 239, n. 2, p. 421-435, 2014. http://dx.doi.org/10.1007/s00425-013-1987-9 ZHANG, Z. X.; TIAN, X.; BAI, Y.; LIU, H.; NIU, X.; WANG, Z.; WANG, Q. Field Sandbur (Cenchrus pauciflorus) Seeds in the Same Bur Respond Differently to Temperature and Water Potential in Relation to Germination in a Semi-Arid Environment, China. Plos One, v. 11, n. 12, p. 168-394, 19 dez. 2016. http://dx.doi.org/10.1371/journal.pone.0168394 ZHANG, Z. X.; ZHANG, K.; TIAN, X. Characteristics of biological components of Cenchrus pauciflorus under wet and dry habitats. Pratacult Science, v. 12, p. 21, 2012. http://en.cnki.com.cn/Article_en/CJFDTOTAL-CYKX201212021.htm This is an open access article distributed under the terms of the Creative Commons license.