Distribution of invasive exotic species Artocarpus heterophyllus Lam. in a forest fragment in the Amazon

Artocarpus heterophyllus is an invasive exotic species known for its negative impacts on Brazilian ecosystems. The aim of this study was to evaluate the distribution and population structure of A. heterophyllus in the plant community of a forest fragment in the Amazon. Individuals of this species were subject to active search at Sumaúma State Park, in Manaus, and two plots were delimited, where these individuals were counted. In each plot, the jackfruit tree individual with the largest Diameter at Breast Height (DBH) was centralized, and from it, native species were inventoried. The parameters of relative density, relative dominance and the importance value index were estimated. Jackfruit tree individuals in the plots had grouped distribution and their number in plots 1 and 2 was 308 and 872 individuals, respectively. In quadrant 1, 254 jackfruit trees and 118 native individuals were recorded, and in quadrant 2, 629 jackfruit and 130 native individuals. The jackfruit tree reached indices higher than the sum of the phytosociological indices of all native species. Jackfruit tree distribution was considered similar to that occurring in other already invaded areas of Brazil, which may indicate that the same impacts may occur in Amazonian ecosystems.


Introduction
Changes in land use are increasingly intense in the Amazon region; it is estimated that 20% of the biome has already been devastated and deforestation has continued to rise since the last decade (Rutt et al., 2019). Concurrently, there is a lack of information on the presence of invasive exotic species in the North of Brazil, due to the low number of academic publications in this field (Santos et al., 2021). The scarcity of studies does not mean that invasive species are not present or that the risks and impacts of biological invasions are not a reality.
One of the examples of exotic species commonly cultivated in the Amazon is Artocarpus heterophyllus Lam.
(Moraceae) (Falcão et al., 2001), popularly known as jackfruit tree, native to the tropical forests of Malaysia and India. It is a large and evergreen tree, with latex in all its organs, reaching up to 20 meters in height, with rapid growth in its early years, attaining a 1.5 m rate per year and decreasing to 0.5 m per year when it reaches maturity (Prakash et al., 2009). Within its genus, A. heterophyllus is the most widespread, useful and also the most adaptable species (Elevitch & Manner, 2006). Due to its food use, the jackfruit tree was introduced in Brazil in the 17th century, and was later used in reforestation projects in the state of Rio de Janeiro (Pereira & Kaplan, 2013). Today, the jackfruit tree is widely distributed throughout the Brazilian territory and is known as an aggressive invasive exotic species in the Atlantic Forest of the Northeast and Southeast of Brazil (Fabricante et al., 2012;Moura et al., 2020). In addition, according to the national database on exotic species, jackfruit trees are present in 12 states (Hórus Institute, 2021). As a result, the environmental impacts arising from the biological invasion of A. heterophyllus include negative changes on the richness, diversity and soil of the invaded areas (Fabricante et al., 2012).
Considering A. heterophyllus important threat to native vegetation, making management and control actions are necessary (Fabricante et al., 2012). The biological invasion of jackfruit trees can be facilitated on account of its ease of adaptation to a wide range of humid tropical environments (Elevitch & Manner, 2006). Studies involving A. heterophyllus and its relationships with native Amazonian species allow for a better understanding of the future scenario of biological invasions in the Amazon and its possible impacts, in addition to promoting adequate management actions to control it. Thus, our aim was to evaluate the distribution and population structure of A. heterophyllus in the plant community of a forest fragment in the Amazon region. Research, Society andDevelopment, v. 11, n. 3, e59011326734, 2022 (CC BY 4.0) | ISSN 2525-3409 | DOI: http://dx.doi.org/10.33448/rsd-v11i3.26734 3 2. Methodology

Study area
The study was carried out in the city of Manaus, Amazonas, Brazil, at Sumaúma State Park (03°01'50" S / 59°58'59" W), a forest fragment with a 52.57 ha area, considered a remnant of lowland tropical rainforest, predominantly in the secondary succession stage and with campinarana patches. The Park does not have a history of controlling and managing the A.
heterophyllus population or other exotic species, it is a forest edge and an urban park, its boundaries make contact with backyards of homes, some of which have jackfruit trees grown inside them, and which may have an influence on the dispersion of the species into the conservation unit (Magalhães et al., 2020).

Delimitation of biologically invaded areas by jackfruit trees
From November to December 2018, active searches were carried out for jackfruit tree individuals in the entire perimeter of the Park's forest edges and trails. The occurrence of such species was identified in four areas, two of them only had one adult individual each. The other two areas, plots (P1 and P2) were set up for population sampling, as a greater number of individuals was found ( Figure 1). The methodology used in this study was based on the studies by Fabricante et al., (2012). To verify the distribution of jackfruit trees and native species within each plot, the jackfruit tree individual with the highest DBH was chosen as a matrix. From the centralized matrix jackfruit tree, a quadrant equivalent to the projection of the tree canopy on the ground was delimited, considering that jackfruit trees exert direct influence on the individuals below their canopy (Abreu & Rodrigues, 2010). The two quadrants (Q1 and Q2), referring to plots 1 and 2 respectively, measured 18 x 18 m and 20 x 20 m.
The jackfruit tree individuals and the native species present in the quadrants, whose stems rose above 1.30 m from the ground for DBH measurement, were sampled to calculate the phytosociological variables of relative density, relative dominance and importance value index (Moro & Martins, 2011). The other individuals, including native herbaceous plants and seedlings, were counted and mapped according to their distance from the matrix jackfruit tree.

Identification of native species
The botanical identification of native species was carried out by collecting parts of plant organs, preferably fertile ones. All collected material was oven-dried at 60 °C for 48 to 72 hours. Afterwards, their identification was confirmed with the help of specialists and compared with exsiccates. The origin and area of occurrence of the species were obtained from botanical guides (e.g. Ribeiro et al., 1999;Souza & Lorenzi, 2008) and online databases. All the plant material collected was deposited in the Laboratory of Applied Ecology at Amazonas State University.

Results
Jackfruit tree individuals showed predominantly grouped distribution, visually forming a monodominant population in the plots (Figure 2). In plot 1, the total number of jackfruit trees observed was 200, with DBH ranging from 0.7 to 34 cm. In plot 2, a total of 336 jackfruit trees were observed, with DBH ranging from 0.7 to 100.6 cm. The total number of jackfruit accounted for in the two areas was 1.180. Considering the entire population in the plots there were 524 juvenile individuals, 5 pre-reproductive individuals and 7 adult individuals, ages determined by the diameters of each individual of the population.
The seedlings totalized 644 individuals, 108 in P1 and 536 in P2. Considering only the areas of the quadrants and the inclusion of native species, quadrant 1 (Q1) had 118 individuals in total, distributed in 42 species; in addition to 254 jackfruit (including seedlings). In quadrant 2 (Q2), 130 individuals were observed, distributed in 48 species; with 629 jackfruit (including seedlings). In Q1, the native species with the highest importance value index was Ficus maxima (6.5%) and the greatest abundance of native individuals was Lauraceae NI 1, with five individuals, followed by F. maxima, with three. In Q2, the highest IVI was that of Inga edulis (5.2%), which had seven individuals, being the most abundant among the natives. The estimated phytosociological parameters for jackfruit trees were superior to the set of all native species sampled in the quadrants (Tables 2 and 3).  Regarding the spatial pattern of individuals in the quadrants, it was observed that, in the vicinity of the matrix jackfruit tree, the number of native individuals was smaller, increasing as they distanced themselves from it. For A.
heterophyllus, the observed pattern was the opposite, as most of its individuals were under the matrix canopy. In Q1, only eight individuals, of five species, were about 5 m away from the matrix jackfruit tree, while in Q2, there were only six, of five species, keeping the same distance as that seen in Q1. As the distance from the matrix jackfruit tree increased, the number of native individuals also increased.
In the case of the species inventoried for phytosociological analyses, in Q1 the most abundant species (F.

Discussion
The main characteristic of the jackfruit tree populations in the invaded areas was their grouped distribution, with the development of monodominant settlements. This distribution pattern, in which younger individuals surround adults, was also observed by Freitas et al., (2017), in the Atlantic Forest. In the same study, the Importance Value Index of A. heterophyllus was 35.62% and surpassed the values of all native species in the community (Freitas et al., 2017). The same was true for Sumaúma Park, as the sum of the phytosociological parameters of all natives was inferior to that of the jackfruit trees. This situation shows the dominance of jackfruit trees over the native plant community and one of the negative effects of its biological invasion. This was also made clear by the number of native individuals versus jackfruit tree individuals; for example, in Q2, the total number of jackfruit trees was five times that of the natives.
At Sumaúma Park, the plots that cover the jackfruit tree occupation area were located on the forest edge, which may have favored its expansion, since few species are capable of invading advanced succession stages, especially in tropical forests (Fine, 2002). As a result, the jackfruit trees chosen as matrices were located very close to the areas where this species was already cultivated even before the Park was established, which may have acted as a source of propagules for its interior.
Fruit production is also one of the factors that help to understand the establishment and propagation of the species. It is estimated that a jackfruit tree can produce up to 100 fruits per year (Lalmuanpuii et al., 2018), and seed dispersal occurs by barocoria (Novelli et al., 2010), allowing it to reach and colonize more distant areas. Most of the jackfruit tree individuals at Sumaúma Park were juveniles and, probably, the population is booming, considering that many individuals were yet to become reproductive. At Tijuca National Park, the largest proportion of individuals (70%) also belonged to the first diametric classes -Juveniles DBH ≤ 15 cm (Abreu & Rodrigues, 2010). This situation shows that the number of areas subject to biological invasion can further increase over time.
The positive interactions with the resident fauna can favor the success of invasive species, through greater reproductive success and colonization of new areas (Taconi & Pires, 2021). Regarding the fruits, jackfruit trees are also associated with small Atlantic Forest mammals, such as the Didelphis aurita (opossum), Trinomys dimidiatus (bristly mouse), Cuniculus paca (paca) (Raíces et al., 2017) and Leontopithecus chrysomelas (golden-headed lion tamarin) (Oliveira et al., 2011). All of them were recorded feeding on the mesocarp and carrying the seeds (Oliveira et al., 2011;Raíces et al., 2017), which can influence the dispersion of the species and represent one of the main negative impacts for the protected areas.
Sumaúma Park has two populations of the pied tamarin (Saguinus bicolor) (Gordo et al., 2019), and recorded jackfruit consumption by these primates, which may further contribute to the dispersal of jackfruit trees (e.g., M Gordo unpubl. res.).
Also noteworthy is the occurrence of a species similar to Didelphis aurita, the opossum D. marsupialis (cf.), potentially also a disperser of jackfruit trees (Amazonas, 2009).
Jackfruit tree invasiveness may also be related to allelopathy, a process capable of suppressing germination and/or the establishment of competing species by means of the production of secondary metabolites (Hierro & Callaway, 2003). The relationship between allelopathy and invasive success was demonstrated in Centaurea maculosa, in which allelochemicals exuded by their roots in the invaded area were found to have negative effects on their competitors, with little effect in their native region (Thorpe et al., 2009). This may also explain why some invasive species become more abundant in invaded areas than in their native habitats establishing monodominant settlements (Hierro & Callaway, 2003). In its native environment, jackfruit tree density is low, reaching, on the other hand, high densities in invaded areas (Prakash et al., 2009).
The allelopathy of A. heterophyllus has already been studied, laboratory tests showed that aqueous extracts of the pulp and dry green leaves of jackfruit trees inhibited the germination of Lactuca sativa (lettuce) seeds (Perdomo & Magalhães, 2007). The ethanol extract of A. heterophyllus leaves also reduced the germination speed index of L. sativa and Urochloa brizantha (Costalonga & Batitucci, 2020).
As for the impacts of the biological invasion of jackfruit trees at Tijuca National Park, in Rio de Janeiro, the species is considered the most aggressive invasive species, causing a reduced native plant biodiversity (Abreu & Rodrigues, 2010). In the Atlantic Forest of the Northeast, the species effectively alters the richness of species, the diversity of vegetation and the soils of the invaded sites (Fabricante et al., 2012).

Conclusion
In Sumaúma State Park, we were able to confirm the potential invasive effect of A. heterophyllus in Amazonian environments. The distribution patterns similar to those occurring in other densely invaded areas in the Brazil, both in terms of aggregated distribution and distance of some native species individuals from jackfruit trees, which may indicate that the same negative impacts may occur in Amazonian ecosystems. Finally, considering this scenario, we recommend that jackfruit trees have strict management, especially in protected areas and their borders. New studies on their relationships with native plant and animal species, and allelopathy, are necessary developed to increase the understanding of invasions and their impacts on the natural areas. Further research should also investigate the allelopathic potential of jackfruit under field conditions and the influence on native species, in addition to identifying the substances involved in a possible chemical inhibition.