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Morphometry of the fruits of Genipa americana (Rubiaceae): a case study from the southern coast of Bahia, Brazil

Abstract

We conducted a study to assess the morphometric attributes of Genipa americana fruit, and their relationship with variations in elevation and distances between sampling sites on the southern coast of Bahia, Brazil. Eight fruit were used per sampling site (ten sites; n = 80). Mantel’s test revealed that the spatial distance between sample sites, and elevation of all sampling sites were significantly correlated with the similarities found in fruit diameter (DF), fruit length (FL), and fresh fruit mass (FFM), but the spatial distance between sites, independently of the elevation, was only correlated with the number of seeds per fruit (NSF) and total fresh mass of seeds per fruit (FMSF). The morphometric attributes of fruits, and their associated relationships with elevation and distance between sampling sites are demonstrated.

Key words
Brazilian Atlantic Forest; elevation; native species; spatial distance

Resumo

Nós conduzimos um estudo com o objetivo de acessar os atributos morfométricos de frutos de Genipa americana e suas semelhanças associadas a elevação e distância entre locais de coleta no Litoral Sul da Bahia, Brasil. Foram utilizados oito frutos por local de amostragem (dez locais; n = 80). O teste de Mantel revelou que a distância espacial e a elevação de todos os locais de amostragem estavam significativamente correlacionadas com as semelhanças encontradas no diâmetro do fruto (DF), comprimento do fruto (FL) e massa fresca do fruto (FFM), mas a distância espacial apenas se correlacionou com o número de sementes por fruto (NSF) e a massa fresca total de sementes por fruto (FMSF). Foi demonstrado que os atributos morfométricos de frutos e suas semelhanças associadas na elevação e distância entre os locais de amostragem.

Palavras-chave
Mata Atlântica Brasileira; elevação; espécies nativas; distância espacial

Introduction

Genipa americana L. (Rubiaceae) is a neotropical tree with a wide distribution in the Brazilian territory. It is known as “genipapo” in Portuguese, “iá-nipaba” in Tupi-Guarani, or “genipap” in English. Genipa americana fruits are of the globose berry type, measure 6–8 cm in diameter, weigh 200–400 g, and have a slightly fermented odor when ripe (Lorenzi 2008Lorenzi H (2008) Árvores brasileiras: manual de identificação e cultivo de plantas arbóreas nativas do Brasil. Instituto Plantarum, Nova Odessa. 384p.). Because they are fleshy and juicy, they can be consumed in natural or processed form. They are used by the food industry when manufacturing sweets, juices, and liqueurs (Prudente 2002Prudente RM (2002) Jenipapo. In: Vieira Neto RD (ed.) Frutíferas potenciais para os tabuleiros costeiros e baixadas litorâneas. Embrapa Tabuleiros Costeiros. Empresa de Desenvolvimento Agropecuário de Sergipe, Aracaju. 216p.). Thus, the fruit has great socio-economic importance in some parts of northeastern Brazil (Magistrali et al. 2013Magistrali PR, Faria JAC, Rocha JM & Gasparin E (2013) Physiological behavior of G. americana L seeds regarding the capacity for desiccation and storage tolerance. Journal of Seed Science 4: 495-500.; Virgens et al. 2019Virgens PBS, Conceição TA & Barbosa RM (2019) Tetrazolium test to evaluate viability and vigour in Genipa americana seeds. Seed Science and Technology 47: 307-318. ). The fruit stands out as having a pleasant taste and can be used to treat numerous diseases (Rezende 2010Rezende LC (2010) Avaliação da atividade antioxidante e composição química de seis frutas tropicais consumidas na Bahia. Dissertação. Universidade Federal da Bahia, Salvador. 106p.). Some studies report that these characteristics are related to the antioxidant activity of vitamins and bioactive compounds, such as monoterpenes and flavonoids (Seifried et al. 2007Seifried HE, Anderson DE, Fisher EI & Milner JA (2007) A review of the interaction among dietary antioxidants and reactive oxygen species. The Journal of Nutritional Biochemistry 18: 567-579. ; Santana-Neta 2014Santana-Neta LG (2014) Caracterização e avaliação do potencial de bioativos e atividades antioxidantes de Genipa americana L. desidratado. Dissertação de Mestrado. Universidade Federal da Bahia, Salvador. 79p.; Rezende 2010Rezende LC (2010) Avaliação da atividade antioxidante e composição química de seis frutas tropicais consumidas na Bahia. Dissertação. Universidade Federal da Bahia, Salvador. 106p.). Genipa americana is a very hardy, and fast-growing species, with commercially important fruit and wood (Lorenzi 2008Lorenzi H (2008) Árvores brasileiras: manual de identificação e cultivo de plantas arbóreas nativas do Brasil. Instituto Plantarum, Nova Odessa. 384p.; Rolim et al. 2019Rolim SG, Piña-Rodrigues FCM, Piotto D, Batista A, Freitas MLM, Brienza Junior S, Zakia MJB & Calmon M (2019) Research gaps and priorities in silviculture of native species in Brazil. Working Paper. WRI Brasil, São Paulo, Brasil. Available at <https://wribrasil.org.br/pt/publicacoes>. Access on 3 April 2020
https://wribrasil.org.br/pt/publicacoes...
). Because of these characteristics, G. americana can be an excellent choice for cultivation in agroforestry systems on small farms in the tropics (Montagnini et al. 2004Montagnini F, Cusack D, Petit B & Kanninen M (2004) Environmental services of native tree plantations and agroforestry systems in Central America. Journal of Sustainable Forestry 21: 51-67. ).

According to Ducke (1946)Ducke A (1946) Plantas de cultura pré-colombiana na Amazônia Brasileira. Notas sobre as espécies ou formas espontâneas que supostamente lhes teriam dado origem. Boletim Técnico 8, Instituto Agronômico do Norte 8: 1-24. and Moraes et al. (1994)Moraes VHF, Muller CH, Souza AGC & Antônio IC (1994) Native fruit species of economic potential from the Brazilian Amazon. Angewandte Botanik 68: 47-52., G. americana is probably native to Amazonian regions with alluvial and periodically flooded soils. Historical reports indicate that its fruit was consumed and used for body paintings by indigenous people along the Brazilian Atlantic rainforests before European colonization (Filgueiras & Peixoto 2002Filgueiras TS & Peixoto AL (2002) Flora e vegetação do Brasil na carta de Caminha. Acta Botanica Brasilica 16: 263-272.; Tomchinsky & Ming 2019Tomchinsky B & Ming LC (2019) As plantas comestíveis no Brasil dos séculos XVI e XVII segundo relatos de época. Rodriguésia 70: 03792017.). For example, of the reports from 18 authors who visited Brazil in the 16th and 17th centuries [compiled by Tomchinsky & Ming (2019)Tomchinsky B & Ming LC (2019) As plantas comestíveis no Brasil dos séculos XVI e XVII segundo relatos de época. Rodriguésia 70: 03792017.], 13 cited G. americana as a plant Brazilians used as food. Tomchinsky & Ming (2019)Tomchinsky B & Ming LC (2019) As plantas comestíveis no Brasil dos séculos XVI e XVII segundo relatos de época. Rodriguésia 70: 03792017. also reported that after M. esculenta (manioc), G. americana, Ananas comosus L. (Merr.) (pineapple), and Ipomoea batatas L. (Lam.) (sweet potato) were the plants most commonly referenced for food use in Brazil during the 16th/17th centuries.

Located in the Brazilian Atlantic rainforest, the southern coastal region of the state of Bahia is characterized by its proximity to the Atlantic Ocean and has a typically humid, tropical climate (Mori et al. 1983Mori SA, Boom BM, Carvalho AM & Santos TS (1983) Southern Bahian moist forests. The Botanical Review 49: 155-232. ). In addition, this region’s topography has marked variations in elevation, characterized by the presence of several mountains reaching approximately 1,000 m above sea level (masl) (Amorim et al. 2009Amorim AM, Jardim JG, Lopes MMM, Fiaschi P, Borges RAX, Perdiz RO & Thomas WW (2009) Angiosperms of Montane Forest areas in southern Bahia, Brazil. Biota Neotropica 9: 313-348.; Thomas et al. 2009Thomas WW, Jardim JG, Fiaschi P, Mariano Neto E & Amorim AM (2009) Composição florística e estrutura do componente arbóreo de uma área transicional de Floresta Atlântica no sul da Bahia, Brasil. Acta Botanica Brasilica 32: 65-78. ; Rocha & Amorim 2012Rocha DSB & Amorim AMA (2012) Heterogeneidade altitudinal na Floresta Atlântica setentrional: um estudo de caso no sul da Bahia, Brasil. Acta Botanica Brasilica 26: 309-327.). This region has been inhabited by indigenous people for thousands of years, and by Europeans since the beginning of the 16th century (Cerqueira & De Jesus 2017Cerqueira CA & De Jesus CM (2017) O território litoral sul. In: Ortega AC & Pires MJS (orgs.) As políticas territoriais rurais e a articulação governo federal e estadual: um estudo de caso da Bahia. IPEA, Brasília. Pp. 185-212.). Despite being affected by anthropogenic disturbances for centuries, southern Bahia still has one of the greatest diversities of tree species in the world (Martini et al. 2007Martini AMZ, Fiaschi P, Amorim AM & Paixão JL (2007) A hot-point within a hot-spot: a high diversity site in Brazil’s Atlantic Forest. Biodiversity and Conservation 16: 3111- 3128. ). In southern Bahia, as well as in other parts of northeastern Brazil, the fruits of G. americana have been consumed for centuries in the form of fresh fruits, sweets, or liquors, which are much appreciated during the traditional June festivities. Even today however, the exploitation of G. americana occurs mainly in an extractive way, through the actions of small farmers, without the use of technology or agronomic practices. Interestingly, in southern Bahia, Brazil this species is not found in primary or secondary forests (e.g., Mori et al. 1983Mori SA, Boom BM, Carvalho AM & Santos TS (1983) Southern Bahian moist forests. The Botanical Review 49: 155-232. ; Martini et al. 2007Martini AMZ, Fiaschi P, Amorim AM & Paixão JL (2007) A hot-point within a hot-spot: a high diversity site in Brazil’s Atlantic Forest. Biodiversity and Conservation 16: 3111- 3128. ; Piotto et al. 2009Piotto D, Montagnini F, Thomas W, Ashton M & Oliver C (2009) Forest recovery after swidden cultivation across a 40-year chronosequence in the Atlantic forest of southern Bahia, Brazil. Journal of Plant Ecology 205: 261-272.; Thomas et al. 2009Thomas WW, Jardim JG, Fiaschi P, Mariano Neto E & Amorim AM (2009) Composição florística e estrutura do componente arbóreo de uma área transicional de Floresta Atlântica no sul da Bahia, Brasil. Acta Botanica Brasilica 32: 65-78. ) and is generally found sub-spontaneously in areas close to human settlements, such as cocoa rustic agroforest systems (Sambuichi et al. 2012Sambuichi RHR, Vidal DB, Piasentin FB, Jardim JG, Viana TG, Menezes AA, Mello DLN, Ahnert D & Baligar VC (2012) Cabruca agroforests in southern Bahia, Brazil: tree component, management practices and tree species conservation. Biodiversity and Conservation 21: 1055-1077.), traditional home gardens, and abandoned pastures. This trend in location may be evidence that the species is not native to this region, but instead may have been spread by indigenous people on a dispersion route that began in the Amazon to the south of Brazil.

Morphometric variations of tree fruits have been associated with differences in elevation and soil characteristics, even on small spatial scales (Itoh et al. 2003Itoh A, Yamakura T, Ohkubo T, Kanzaki M, Palmiotto PA, LaFrankie JV, Ashton PS & Lee HS (2003) Importance of topography and soil texture in the spatial distribution of two sympatric dipterocarp trees in a Bornean rainforest. Ecological Research 18: 307-320. ; Davies et al. 2005Davies SJ, Tan S, Lafrankie JV & Potts MD (2005) Soil-related floristic variation in a hyperdiverse dipterocarp forest in Lambir Hills, Sarawak. In: Roubik DW, Sakai S & Hamid A (eds.) Pollination ecology and the rain Forest diversity. Sarawak Studies. Springer-Verlag, New York. Pp. 22-34.). Elevation integrates and defines several physical variables, such as soil texture, and nutrient concentrations (Daws et al. 2002Daws MI, Mullins CE, Burslem DFRP, Paton SR & Dalling JW (2002) Topographic position affects the water regime in a semideciduous tropical forest in Panamá. Plant and Soil 238: 79-90.; Costa et al. 2005Costa FRC, Magnusson WE & Luizao RC (2005) Mesoscale distribution patterns of Amazonian understorey herbs in relation to topography, soil and watersheds. Journal of Ecology 93: 863- 878. ; John et al. 2007John R, Dalling JW, Harms KE, Yavitt JB, Stallard RF, Mirabello M, Hubbell SP, Valencia R, Navarrete H, Vallejo M & Foster RB (2007) Soil nutrients influence spatial distributions of tropical tree species. Proceedings of the National Academy of Sciences 104: 864- 869. ; Quesada et al. 2009Quesada CA, Lloyd J, Schwarz M, Baker TR, Phillips OL, Patino S, Czimczik C, Hodnett MG, Herrera R, Arneth A, Lloyd L, Silveira M, Priante Filho N, Jimenez EM, Paiva R, Vieira I, Neill DA, Silva N, Penuela MC, Monteagudo A, Vasquez R, Prieto A, Rudas J, Fyllas NM, Alvarez Davila E, Erwin T, di Fiore A, Chao KJ, Honorio E, Killeen T, Pena Cruz A, Pitman N, Nu´nez Vargas P, Salomao R & Ram´ırez H (2009) Regional and large-scale patterns in Amazon Forest structure and function are mediated by variations in soil physical and chemical properties. Biogeosciences Discussions 6: 3993-4057. ). The relationships between elevation, vegetation, and soil have always been determinants of ecological processes (Dearborn & Danby 2017Dearborn KD & Danby RK (2017) Aspect and slope influence plant community composition more than elevation across forest-tundra ecotones in subarctic Canada. Journal of Vegetation Science 28: 595- 604. ; Román-Sánchez et al. 2018Román-Sánchez A, Vanwalleghem T, Peña, Laguna A & Giráldez JV (2018) Controls on soil carbon storage from topography and vegetation in a rocky, semi-arid landscapes. Geoderma 311: 159-166. ; Sanaei et al. 2018Sanaei A, Chahouki MAZ, Ali A, Jafari M & Azarnivand H (2018) Abiotic and biotic drivers of aboveground biomass in semi-steppe rangelands. Science of the Total Environment 615: 895-905. ). At the regional scale, spatial heterogeneity in vegetation and soil is attributed to variations in topography and climate (Lybrand & Rasmussen 2015Lybrand RA & Rasmussen C (2015) Quantifying climate and landscape position controls on soil development in semiarid ecosystemsSoil Science Society of America Journal 79: 104-116.). On a local scale, topographic factors such as slope, and slope aspect, can significantly influence vegetation, thereby affecting radiation, temperature, water, and nutrients (Ranney et al. 2015Ranney KJ, Niemann JD, Lehman BM, Green TR & Jones AS (2015) A method to downscale soil moisture to fine resolutions using topographic, vegetation, and soil data. Advances in Water Resources 76: 81- 96. ; Dearborn & Danby 2017Dearborn KD & Danby RK (2017) Aspect and slope influence plant community composition more than elevation across forest-tundra ecotones in subarctic Canada. Journal of Vegetation Science 28: 595- 604. ). Topographic factors have important effects on vegetation dynamics (Bernards & Morris 2017Bernards SJ & Morris LR (2017) Influence of topography on long-term successional trajectories in canyon grasslands. Applied Vegetation Science 20: 236- 246. ; Dearborn & Danby 2017Dearborn KD & Danby RK (2017) Aspect and slope influence plant community composition more than elevation across forest-tundra ecotones in subarctic Canada. Journal of Vegetation Science 28: 595- 604. ; Méndez-Toribio et al. 2017Méndez-Toribio M, Ibarra-Manríquez G, Navarrete-Segueda A & Paz H (2017) Topographic position, but not slope aspect, drives the dominance of functional strategies of tropical dry forest trees. Environmental Research Letters 12: 085002. ). Variations in the topography of ecosystems influence the responses of plant species and functional groups to increased elevation. Thus, topography is expected to affect the morphological diversity of genipap fruit along the south coast of Bahia.

Because G. americana is still managed as a sub-spontaneous tree, and very little is known about its desirable agronomic characteristics, the objective of this study was to assess the morphometric attributes of G. americana fruits and their associated relationship with elevation and distance between sampling sites in the southern coast of Bahia, Brazil.

Materials and Methods

Study area and collection of plant material

The study was carried out in the citizenship territory of the southern coast of Bahia (CTSB). The CTSB is composed of 26 municipalities, with a total area of 14,664.54 km2 and approximately 772,683 inhabitants (Cerqueira & De Jesus 2017Cerqueira CA & De Jesus CM (2017) O território litoral sul. In: Ortega AC & Pires MJS (orgs.) As políticas territoriais rurais e a articulação governo federal e estadual: um estudo de caso da Bahia. IPEA, Brasília. Pp. 185-212.). Per Köppen’s classification (Alvares et al. 2013Alvares CA, Stape JL, Sentelhas PC & Gonçalves JL (2013) Modeling monthly mean air temperature for Brazil. Theoretical and Applied Climatology 113: 407- 427. ), the region is a humid (or super-humid) tropical climate of the Af type, does not have a dry season, and has an average monthly temperature of 24–26 °C. The total rainfall exceeds 1,500 mm annually, with the greatest rainfall from March–August, and even the driest month receives over 60 mm of rainfall. In the warmer months (January and February) the temperature is 24–25 °C.

Fruits from G. americana were collected from where they were spontaneously growing on small rural properties, and from open markets in different areas of the CTSB (Fig. 1). Collections were carried out from April–July 2019 from ten sites throughout six municipalities (Ilhéus - 1,760.0 km2, Itabuna - 432.2 km2, Buerarema - 230,5 km2, São José da Vitória - 72.5 km2, Ibicaraí -231.9 km2, and Jussari - 356.8 km2), within a total area of 3,083.9 km2 and an elevation gradient of 29–400 masl (Tab. 1). The latitude and longitude of the different sample sites were obtained using a GPS (Global Positioning System). Only healthy and fully ripe fruit were used. Maturation was determined when a natural separation of the fruit and branch occurred, or when a healthy fruit was found in the soil of the sampling site (without herbivory and deformation to the pericarp, or other visible damage). The fruits, once harvested and/or purchased (with the same characteristics as above), were packed in plastic boxes and transferred to the Plant Physiology Laboratory of the Universidade Estadual de Santa Cruz (UESC), Ilhéus, Bahia, Brazil, for later measurements.

Figure 1
Collection areas of the fruits of Genipa americana in southern Bahia, Brazil. Sampling sites: S1 to S10.
Table 1
Characteristics of the collection areas of the fruits of Genipa americana, in southern Bahia, Brazil.

Measurement of phenotypic morphometric attributes of fruits

For eight fruit per sampling site were used (ten sites: S1 to S10; n = 80). We measured fruit diameter (FD, cm), fruit length (FL, cm), fresh fruit mass (FFM, g), the number of seeds per fruit (NSF), total fresh mass of seeds per fruit (FMSF, g), total dry mass of seeds per fruit (DMSF, g), and the mass of 1,000 seeds (MTS, g). FL was measured from the base to the apex, and FD was measured on the median line (accuracy ± 0.1 mm). After FL and FD measurements, the fruits were pulped, and the seeds were immediately washed in water and dried with paper towels to obtain FMSF. Fruit and seed weights were obtained using an analytical balance accurate to ± 0.001 g. The DMSF was obtained after the seeds were dried on paper towels in the shade at room temperature for approximately one week. Based on the values of FMSF and DMSF the average water content of the seeds in fresh fruits was approximately 82%. Finally, the MTS was calculated in order to estimate the mass of seeds in fresh fruits. The MTS was calculated from the equation adapted from the Ministry of Agriculture and Supply’s seed analysis rules (Mapa 2009Mapa (2009) Regras para análise de sementes. Ministério da Agricultura, Pecuária e Abastecimento, Brasília. 399p.): MTS = (1,000 × FMSF) / NSF.

Data analysis

All variables were evaluated using analysis of variance (Fisher’s test) or Kruskal-Wallis for the factor: sampling site (S1 to S10). Bonferroni’s tests were applied to compare the means between sampling sites. All statistical assumptions were checked. Spearman (rs ), or Pearson (rρ ) correlation coefficients between all pairs of variables were calculated. Mantel’s test correlations (rm ) were made, contrasting the similarities of the phenotypic morphometric attributes of fruit and seeds, with the spatial distances (km) between sites, and the similitude of sample site elevations. These similarities were calculated by the differences of the variables between two sampling sites in a comparison matrix; the spatial separation was calculated by Euclidean distance. The elevation was defined by calculating the average value in a diameter of 1 km around each sampling point (S1 to S10), using ArcGIS version 10.7.1. The Mantel test was calculated with permutations of the Monte-Carlo test method (n = 2000 interactions). This test measures the correlation between two matrices (biological variable and spatial distance), and is one way of testing for spatial autocorrelation (Crabot et al. 2019Crabot J, Clappe S, Dray S & Datry T (2019) Testing the Mantel statistic with a spatially-constrained permutation procedure. Methods in Ecology and Evolution 10: 532-540. ; Giraldo Caballero & Camacho-Tamayo et al. 2018Giraldo R, Caballero W & Camacho-Tamayo J (2018) Mantel test for spatial functional data. AStA Advances in Statistical Analysis 102: 21-39. ). All statistical analyses were performed using R programming language version 3.6.1, (RCoreTeam 2019) with a significance level of α = 0.05.

To assess the divergence between sites (S), a cluster analysis was performed. The distance matrix of that analysis was calculated using the Euclidean dissimilarity Gower (1985)Gower JC (1985) Properties of Euclidean and non-Euclidean distance matrices. Linear Algebra and its Applications 67: 81- 97. measure, and Ward’s grouping method (Ward 1963Ward JH (1963) Hierarquical grouping to optimize an objective function. Journal of the American Statistical Association 58: 236 - 244. ). The definition of the group number was established using the pseudo t2 index (Duda & Hart 1973Duda RO & Hart PE (1973) Pattern classification and scene analysis. John Wiley & Sons, New York. 512p.). In order to efficiently visualize the relationship between biometric variables and sites, a heat map was constructed. We used red, white, and blue color palettes. The colors are referenced according to the average values of each variable, considering all the sites studied. The red and blue colors indicate values above and below the average, respectively, and the white color relates to values similar to the average. All analyses were performed using R software (R Core Team 2019R Core Team (2019) R: a language and environment for statistical computing. Available at <https://www.r-project.org/>. Access on 19 January 2020.
https://www.r-project.org/...
).

Results

All morphometric attributes of fruit showed significant differences between sampling sites (S1 to S10), ordered from lowest to highest elevation (Fig. 2). Despite this finding, no pair of variables showed the same pattern of magnitude between sampling sites. However, significant correlations were found between the elevation of sampling sites and FD, FL, and FFM (rs = 0.56, 0.42, and 0.24, respectively; Fig. 3). As expected, all other variables showed a significant correlation with each other, except for MTS with FFM and FMSF (P > 0.05).

Figure 2
a-h. Phenotypic morphometric attributes of fruits of Genipa americana in southern Bahia, Brazil (n = 8 per sampling sites, S1 to S10) – a. elevation (meters above sea level); b. FD = fruit diameter; c. FL = fruit length; d. FFM = fruit fresh mass; e. NSF = number of seeds per fruit; f. FMSF = total fresh mass of seeds per fruit; g. DMSF = total dry mass of seeds per fruit; h. MST = and mass of 1,000 seeds. Equal letters indicate no statistically significant difference between sampling sites. (P > 0.05, Bonferroni’s test; KW = Kruskal-Wallis test; F = Fisher value; d.f. = 9, 70; R2 = coefficient of determination; ** = P < 0.01; *** = P < 0.001. SE = standard error).
Figure 3
Matrix of relationships between pairs of phenotypic morphometric attributes of fruits of Genipa americana in southern Bahia, Brazil (n = 80). Subplots in the upper diagonal represent the correlation coefficient between pairs of variables (rs and are Spearman and Pearson correlation coefficient, respectively). The subplot on the diagonal shows the probability density curve (Shapiro-Wilks’s test, α = 0.05; Normal distribution, p > 0.05). Subplots in the lower diagonal represent the dispersion between pairs of variables (solid line shows the best fit of a linear regression model). n.s. = not significant; * = P < 0.05; ** = P < 0.01; *** = P < 0.001. The meaning of the abbreviations sees Fig. 2.

Mantel’s test revealed that the spatial distances between, and elevations of, all sampling sites were significantly correlated with the similarities found in FD, FL, and FFM (rm = 0.23, 0.29, and 0.26, respectively; P < 0.001; Tab. 2) , but the spatial distance between sites, independently of the elevation, only correlated with NSF and FMSF (rm = 0.09 and 0.10, respectively; P < 0.05). DMSF and MTS showed no significant correlation with Mantel (P > 0.05).

Table 2
Mantel’s test correlations (rm ) between the similarities of the phenotypic morphometric attributes of fruits vs. the spatial separation and the similarities of elevation of all sampling sites. n.s. = not significant. * = P < 0.05; ** = P < 0.01; *** = P < 0.001. The number of permutations based on Monte-Carlo test were of n = 2000 interactions. The meaning of the abbreviations sees Fig. 2.

Cluster analysis showed the formation of two groups in relation to the sites (S), and two groups in relation to the set of variables. For the sites, group I consisted of sites S1, S2, S3, and S4, and group II of sites S5, S6, S7, S8, S9, and S10. For the variables, group I was formed by the variables FMSF, FFM, DMSF, and NSF, and group II by the variables FD, FL, and MST. Group I sites compared to group II had a lower value for morphometric variables, except for MTS (Fig. 4). In contrast, most sites in group II had low MTS values.

Figure 4
Cluster analysis with heat map in relation to the sites (horizontal axis) and phenotypic morphometric attributes of fruits of Genipa americana in southern Bahia, Brazil. (n = 80) (vertical axis); S = Site.

Discussion

Genipa americana is a neotropical tree, with a wide distribution throughout the Brazilian territory (Judd et al. 2008Judd WS, Campbell CS, Kellogg EA, Stevens PF & Donoghue MJ (2008) Plant systematics: a phylogenetic approach. 3rd ed. Sinauer, Sunderland. 609p.; Souza & Lorenzi 2005Souza VC & Lorenzi H (2005) Botânica sistemática: guia ilustrado para identificação das famílias de Angiospermas da flora brasileira baseado em APG II. Instituto Plantarum, Nova Odessa. 640p.). Because of human use of this species, especially by Brazilian indigenous people, it is likely that its current distribution pattern reflects a complex association between ecological and historical processes. These factors may have contributed to shaping the distribution pattern of G. americana in the area covered by this study, since the variability found in the morphometric attributes associated with the distribution and elevation of the sites was more accentuated when the sites were closer together.

Patterns of forest diversity depend strongly on how tree species are spatially distributed in relation to the environment (Zuleta et al. 2018Zuleta D, Russo ES, Barona A, Barreto-Silva JS, Cardenas D, Castaño N, Davies SJ, Detto M, Sua S, Turner BL & Duque A (2018) Importance of topography for tree species habitat distributions in a terra firme forest in the Colombian Amazon. Plant and Soil 00: 1-17.; Jucker et al. 2018Jucker T, Bongalov B, Burslem DFRP, Nilus R, Dalponte M, Lewis SL & Coomes DA (2018) Topography shapes the structure, composition and function of tropical forest landscapes. Ecology Letters 21: 989-1000. ; Thomas et al. 2015Thomas E, Alcázar Caicedo C, McMichael CH, Corvera R & Loo J (2015) Uncovering spatial patterns in the natural and human history of Brazil nut (Bertholletia excelsa) across the Amazon Basin. Journal of Biogeography 42: 1367-1382. ). The spatial heterogeneity of community structures stems from environmental variables, or community processes (Antonelli et al. 2018Antonelli A, Kissling WD, Flantua SGA, Bermúdez MA, Mulch A, Muellner Riehl AN & Hoorn C (2018) Geological and climatic influences on mountain biodiversity. Nature Geoscience 11: 718 -725.; Badgley et al. 2017Badgley C, Smiley TM, Terry R, Davis EB, Desantis LRG, Fox DL & Yanites BJ (2017) Biodiversity and topographic complexity: modern and geohistorical perspectives. Trends in Ecology & Evolution 3: 211- 226. ). In both cases, spatial distribution has a functional role in ecosystems (Borcard & Legendre 2002Borcard D & Legendre P (2002) All-scale spatial analysis of ecological data by means of principal coordinates of neighbour matrices. Ecological Modelling 153: 51-68.), and is associated with changes in elevation. In our study, we found high variability in the morphometric attributes evaluated between the sampling sites, which may be related to the anthropization of these areas, and the associated variations in elevation. In addition, within the same species there are individual variations owing to the influences of genetic and environmental factors during seed development (Marcos-Filho 2015Marcos-Filho J (2015) Seed vigor testing: an overview of the past, present and future perspective. Scientia Agricola 72: 363- 374.). In the present study, the morphometric variations occurred both within, and between, the different locations, resulting in the formation of two clusters depending on the elevation and morphometric characteristics. The sites with the highest elevations are those that also had the highest morphometric values; in fact, environmental factors also seem to affect the variations found. Several studies have shown that tropical tree species have high variability in fruit size, the number of seeds, and fresh weight of fruit (Braga et al. 2007Braga LF, Sousa MP, Gilberti S & Carvalho MAC (2007) Caracterização morfométrica de sementes de castanha de sapucaia (Lecythis pisonis Cambess - Lecythidaceae). Revista de Ciências Agro-Ambientais 1: 111-116.; Matos et al. 2014Matos FS, Nunes YRF, Silva MAP & Oliveira IS (2014) Variação biométrica de diásporos de buriti (Mauritia flexuosa L.f. - Arecaceae) em veredas em diferentes estágios de conservação. Ciência Florestal 4: 833-842.; Zuffo et al. 2014Zuffo AM, Andrade FR & Zuffo Júnior JM (2014) Caracterização biométrica de frutos e sementes de baru (Dipteryx alata Vog.) na região leste de Mato Grosso, Brasil. Revista de Ciências Agrárias 37: 463-471.; Virgens et al. 2019Virgens PBS, Conceição TA & Barbosa RM (2019) Tetrazolium test to evaluate viability and vigour in Genipa americana seeds. Seed Science and Technology 47: 307-318. ).

Studies have shown that the effects of abiotic factors are more evident at larger spatial scales, while biotic factors are more important at smaller scales (Yang et al. 2016Yang Y, Saatchi SS, Xu L, Yu Y, Lefsky MA, White L, Knyazikhin Y & Myneni RB (2016) Abiotic controls on macroscale variations of humid tropical forest height. Remote Sensing of Environment 8: 494. ; Muscarella et al. 2019Muscarella R, Kolyaie S, Morton DC, Zimmerman JK & Uriarte M (2019) Effects of topography on tropical forest structure depend on climate context. Ecology 00: 1-15.). The spatial variations in ecosystem composition are more evident on larger scales (Jucker et al. 2018Jucker T, Bongalov B, Burslem DFRP, Nilus R, Dalponte M, Lewis SL & Coomes DA (2018) Topography shapes the structure, composition and function of tropical forest landscapes. Ecology Letters 21: 989-1000. ; Muscarella et al. 2019Muscarella R, Kolyaie S, Morton DC, Zimmerman JK & Uriarte M (2019) Effects of topography on tropical forest structure depend on climate context. Ecology 00: 1-15.). However, we found that even on smaller scales, it was possible to observe the effects of environmental factors on variations in morphometric characteristics found between, and within the studied sites. Thus, the size and mass of seeds can vary between plants of the same species (caused by the climatic conditions of the year), and within the same plant (Piña-Rodrigues & Aguiar 1993Piña-Rodrigues FCM & Aguiar IB (1993) Maturação e dispersão de sementes. In: Aguiar IB, Piña-Rodrigues FCM & Figliolia MB (ed.) Sementes florestais tropicais. Abrates, Brasília. Pp. 215-274.). In addition, the number of seeds per fruit can be affected by the climatic conditions of an area, mainly by water availability during flowering (Marcos-Filho 2015Marcos-Filho J (2015) Seed vigor testing: an overview of the past, present and future perspective. Scientia Agricola 72: 363- 374.) affecting the vigor and resistance of storage, as well as the uniformity of the seeds. In tropical forests, at spatial scales smaller than one square kilometer, variation in soil properties can also influence the distribution of tree species (John et al. 2007John R, Dalling JW, Harms KE, Yavitt JB, Stallard RF, Mirabello M, Hubbell SP, Valencia R, Navarrete H, Vallejo M & Foster RB (2007) Soil nutrients influence spatial distributions of tropical tree species. Proceedings of the National Academy of Sciences 104: 864- 869. ) and affect the characteristics of G. americana fruits, as observed in our study.

It should be noted that variations in FMSF may be associated with the high initial water content of the seeds, which reflects the intermediate behavior regarding the storage of G. americana seeds (Carvalho & Nascimento 2000Carvalho UEJ & Nascimento OMW (2000) Sensibilidade de sementes de jenipapo (Genipa americana L.) ao dessecamento e congelamento. (Sensitivity of Genipa americana L. seeds to desiccation and freezing). Revista Brasileira de Fruticultura 22: 53-56. ; Magistrali et al. 2015Magistrali PR, José AC, Faria JMR & Nascimento JF (2015) Slow drying outperforms rapid drying in augmenting the desiccation tolerance of Genipa americana seeds. Seed Science and Technology 43: 101- 110.). The FMFS is also related to the time after extraction of seeds from the fruits (Oliveira et al. 2011Oliveira LM, Silva EO, Bruno RLA & Alves EU (2011) Períodos e ambientes de secagem na qualidade de sementes de Genipa americana L. (Periods of dry environments in the seeds quality of Genipa americana L.). Semina: Ciências Agrárias 32: 495-502.) and the water availability in the environment (Toublanc-Lambault et al. 2019Toublanc-Lambault O, Pouteau R, Davezies M, Marron M, Pain A, Fogliani B & Marmey P (2019) Environmental correlates for seed desiccation sensitivity of New Caledonian plant species. Pacific Science 73: 231-248.). As the FMFS was measured just after the extraction of the seeds from the fruits, the high values of FMFS in our study may explain the higher values of MTS in comparison with similar studies published with G. americana (Paiva-Sobrinho et al. 2017Paiva-Sobrinho S, Albuquerque MCF, Luz PB & Camili EC (2017) Caracterização física de frutos e sementes de Lafoensia pacari, Alibertia edulis e Genipa americana (Physical characterization of fruits and seeds of Lafoensia pacari, Alibertia edulis and Genipa americana). Revista de Ciências Agrárias 40: 71-80. ; Virgens et al. 2019Virgens PBS, Conceição TA & Barbosa RM (2019) Tetrazolium test to evaluate viability and vigour in Genipa americana seeds. Seed Science and Technology 47: 307-318. ). Moreover, considering that the fruits used in our study were collected in areas of the Atlantic forest (in ecosystems with high, regular, and distributed rainfall throughout the year), the climatic characteristics of the areas may have contributed to the high values of FMSF. The high moisture content of fruits and seeds can also be related to the site elevation. As precipitation increases and evapotranspiration decreases with elevation, a higher elevation can result in higher soil and fruit moisture content (Zhu & Lin, 2011Zhu Q & Li H (2011) Influences of soil, terrain, and crop growth on soil moisture variation from transect to farm scales. Geoderma 163: 45-54. ; Wang et al. 2017Wang Z, Hu Y, Wang R, Guo S, Du L, Zhao M & Yao Z (2017) Soil organic carbon on the fragmented Chinese Loess Plateau: combining effects of vegetation types and topographic positions. Soil & Tillage Research 174: 1-5. ). However, significant relationships between elevation with FMSF and TMS were not observed in our study.

Our results showed that native tree species which are not yet domesticated, but are found in areas of anthropization, present highly variable morphometric characteristics, as previously verified for this (and other) species (Virgens et al. 2019Virgens PBS, Conceição TA & Barbosa RM (2019) Tetrazolium test to evaluate viability and vigour in Genipa americana seeds. Seed Science and Technology 47: 307-318. ; Paiva-Sobrinho et al. 2017Paiva-Sobrinho S, Albuquerque MCF, Luz PB & Camili EC (2017) Caracterização física de frutos e sementes de Lafoensia pacari, Alibertia edulis e Genipa americana (Physical characterization of fruits and seeds of Lafoensia pacari, Alibertia edulis and Genipa americana). Revista de Ciências Agrárias 40: 71-80. ; Sangalli et al. 2012Sangalli A, Vieira MC, Scalon SPQ, Zárate NAH, Silva CB & Ribeiro IS (2012) Morfometria de frutos e sementes e germinação de carobinha (Jacaranda decurrens subsp. symmetrifoliolata Farias & Proença), após o armazenamento. Revista Brasileira de Plantas Medicinais 2: 267-275. ; Silva Junior et al. 2012Silva Junior VT, Lima JMGM, Rodrigues CWMS & Barbosa DCA (2012) Erythrina velutina willd. (Leguminosae-Papilionoideae) ocorrente em caatinga e brejo de elevation de Pernambuco: biometria, embebição e germinação. Revista Árvore 36: 247-257.; Zuffo et al. 2014Zuffo AM, Andrade FR & Zuffo Júnior JM (2014) Caracterização biométrica de frutos e sementes de baru (Dipteryx alata Vog.) na região leste de Mato Grosso, Brasil. Revista de Ciências Agrárias 37: 463-471.). Thus, knowledge of the morphometric variations of fruit characteristics is important for the improvement of these characteristics (Gonçalves et al. 2013Gonçalves LGV, Andrade R, Marimon Junior BH, Schossler TR, Lenza E & Marimon BS (2013) Biometria de frutos e sementes de mangaba (Hancornia speciosa Gomes) em vegetação natural na região leste de Mato Grosso, Brasil. Revista Ciências Agrárias 36: 31- 40. ). From a genetic perspective, studying the relationship between fruit and seeds is efficient for understanding the dynamics of the morphometric characteristics of each species (Gonçalves et al. 2013Gonçalves LGV, Andrade R, Marimon Junior BH, Schossler TR, Lenza E & Marimon BS (2013) Biometria de frutos e sementes de mangaba (Hancornia speciosa Gomes) em vegetação natural na região leste de Mato Grosso, Brasil. Revista Ciências Agrárias 36: 31- 40. ; Souza et al. 2016Souza AG, Smiderle OJ, Spinelli VM, Souza RO & Bianchi VJ (2016) Correlation of biometrical characteristics of fruit and seed with twinning and vigor of Prunus persica rootstocks. Journal of Seed Science 38: 322-328. ; Maurya et al. 2015Maurya R, Kumar U, Katiyar R & Yadav HK (2015) Correlation and path coefficient analysis in Jatropha curcas L. Genetika 47: 63-70. ; Zuffo et al. 2016Zuffo AM, Steiner F, Bush A & Zuffo Júnior JM (2016) Physical characterization of fruits and seeds of (Fabaceae) Delonix regia (bojer ex hook.) raf. (Fabaceae - caesalpinoideae). International Journal of Current Research 8: 42072-42076.), as these correlations can help identify which mechanisms are involved in the species’ diversity of expression. In our study, it was possible to observe strong correlations between FL and FD, and between FMSF and MTS. In addition, sites S10, S9, and S7 showed a stronger correlation between these variables than others, and indicate the possibility of developing procedures to estimate the production of seeds for commercial purposes from assessments in the areas of seed collection.

We also demonstrated that fruits of G. americana with different spatial distributions and elevations in the southern region of Bahia showed highly variable morphometric attributes. Differences in the variability of these characteristics can be indicative of the degree of the sites’ anthropization. It should also be noted that exploitation of G. americana in the southern region of Bahia is mainly extractive. However, the commercialization of fruits in the region mainly occurs in open markets, on the edges of highways where species occur, or on rural properties where cocoa is planted based on the cabruca production system, under the shade of native trees such as G. americana. Thus, studies such as this one can inform the selection of native trees in a humid tropical climate based on the morphometric characteristics of fruits, to indirectly select important variables for the conservation or exploitation of the genetic resources of these species.

In summary, all morphometric attributes of fruits showed a significant difference between sampling sites. Significant correlations were found between the elevation of sampling sites and fruit diameter, and fruit length and fresh fruit mass. Mantel’s test revealed that the spatial distance between sites and elevation of all sampling sites were significantly correlated with the similarities found in fruit diameter, fruit length, and fruit fresh mass, but the spatial distance between sites, independently of the elevation, was only correlated with the number of seeds per fruit and total fresh mass of seeds per fruit. The morphometric attributes of fruit and seeds, and their associated similarities in elevation and distance between sampling sites have been demonstrated.

Acknowledgements

This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001. Funding for Catriane Sousa Santos was provided by scholarships from the Fundação de Amparo à Pesquisa do Estado da Bahia (BOL0130/2019). Marcelo S. Mielke (305477/2018-8) and Ândrea C. Dalmolin (307604/2020-9) acknowledge CNPq for fellowships of scientific productivity.

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Edited by

Area Editor: Dr. Joel Campo de Paula

Publication Dates

  • Publication in this collection
    22 Oct 2021
  • Date of issue
    2021

History

  • Received
    27 Apr 2020
  • Accepted
    05 Oct 2020
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