A synopsis of Convolvulaceae from the Upper Turi-Gurupi region in the Amazon of Maranhão, Brazil

A synopsis of Convolvulaceae species from the Upper Turi-Gurupi region, a strategic area for the conservation of Amazonian biodiversity in the Maranhão, is presented. Field samples and herbarium collections were analyzed to build a checklist, indicating the most representative taxa and providing data on growth habit, geographic distribution, occurrence in Brazilian phytogeographic domains, and distribution in the Upper Turi-Gurupi region. Twenty-one species and nine genera ( Aniseia Choisy, Bonamia Thouars, Camonea Raf., Distimake Raf., Evolvulus L., Ipomoea L., Maripa Aubl., Odonellia K.R. Robertson, Operculina Silva Manso) were recorded. Ipomoea was the richest genus (10 species), and I. asarifolia was the most collected species. Maripa scandens is a new record for Maranhão and, in relation to the last taxonomic work of Convolvulaceae in the Amazon, which covered Maranhão, 10 species are new records for the state. A heterogeneous distribution of the species and sampling gaps were observed in the region, pointing to the need for further surveys. This study contributes to the knowledge of Convolvulaceae in the Amazon and stimulates the conservation of the Amazonian flora in Maranhão, since the study area is under risk of biodiversity loss due to environmental degradation and is one of the most threatened in the Amazon.


Introduction
Convolvulaceae Juss. is represented by about 1,900 species and 60 genera with a cosmopolitan distribution, with the largest number of records of species in the tropical region of the globe and few representatives in temperate areas (Mabberley, 1987;Austin, 1998;Staples & Brummitt, 2007;Simões & Staples, this region comprises 18 municipalities and has potential for logging, fishing, agriculture, livestock, tourism and ecotourism activities, besides beekeeping and plant extraction (SEPLAN, 2008). It is also a strategic conservation area in the Amazon domain, with high floristic potential mainly because the Turiaçu River basin and the Gurupi Biological Reserve are within its territory. The Turiaçu River basin is the third largest in the Amazon, with a perimeter of 938.8km and an area of 14,394 km 2 , corresponding to 12.7% of the total territory of this domain (Correia Filho, Gomes, Nunes, & Lopes Filho, 2011;Catunda, & Dias, 2019).
Deforestation and uncontrolled fragmentation in the Amazon of the state of Maranhão reach alarming rates: the original forest cover decreased from 25% (24,700 km²) in 2016 to 24% (23,967 km²) in 2019. This means that the remnaining 6,038 km² of forest have been degraded by fires and/or illegal logging and present no core areas (outside legally protected areas) with the minimum size to ensure sustainable management practices (Silva-Junior et al., 2020).
The objective of this study was to elaborate a synopsis of the Convolvulaceae species occurring in the Upper Turi-Gurupi region compiled through field sampling and analysis of materials previously collected in the area. Our goal is to investigate the floristic diversity of the family, contribute to the increase of botanical knowledge of the area and the state of Maranhão, and fill gaps in the floristic data of the Brazilian Amazon.

Materials and Methods
Collections were carried out in three forest fragments in the municipalities of Zé Doca, Nova Olinda and Centro Novo do Maranhão, within the Upper Turi-Gurupi region ( Figure 1). These municipalities have 2,138.981 km 2 , 2,451.367 km 2 and 8.482,342 km 2 , respectively, of Amazon Forest, corresponding to 9.4% of the total area of this biome in the state (Catunda, & Dias, 2019). Collections in Centro Novo do Maranhão were made within the Gurupi Biological Reserve, an integral protection conservation unit.
Seven field trips were held from May 2019 to October 2021. The random walking method (Filgueiras, Nogueira, Brochado and Guala II, 1994) was used in order to cover most of the phytophysiognomies. Populations in the field were photographed and geographic coordinates and information on the habitat were recorded. The botanical materials of each species were herborized and deposited in the collection of the Prof. Aluísio Bittencourt Herbarium (HABIT) from the Center for Higher Studies of Caxias (CESC/UEMA) and the João Murça Pires Herbarium (MG) from the Emílio Goeldi Museum of Pará (MPEG).
In addition to the samples collected in the field, the the herbaria PEUFR, INPA, IAN, MAR, MG, NY, P and RB (acronyms according to Thiers, 2021), which have collections from the study area, were also consulted. The herbaria SP and MO were consulted, but no records of collections for the study area were found. The accepted names and their correct authorities are in accordance with IPNI (2021) and Flora do Brasil (2020). Data on growth habits, geographic distribution, occurrence in Brazilian phytogeographic domains, and taxa endemic to Brazil based on data from Flora do Brasil (2020) are provided, as well as an identification key for the species. The distribution of taxa in the Upper Turi-Gurupi region was prepared based on geographic information obtained from the collections, noted in the labels of the studied specimens, and maps were generated in the Quantum GIS 3.6 software (Qgis, 2015).

Distimake Raf.
Distimake is characterized by climbing, rarely erect or prostrate subshrubby habit, simple or compound leaves, white or yellow entirely glabrous corollas, stamens with twisted anthers after anthesis, entire styles, globose stigmas, and generally 4-valved capsules with greatly accrescent calyx (Simões, & Staples, 2017). Distimake is widespread in tropical America and tropical Africa, with disjunct species in Asia and northern Australia (Simões, & Staples, 2017). In Brazil, there are 18 species, nine of which are endemic . Five species are reported for the Brazilian Amazon and four for Maranhão . Two species were found in the the Upper Turi-Gurupi region.
Key to species of Distimake from the Upper Turi-Gurupi region
Key to species of Ipomoea from the Upper Turi-Gurupi region Distribution: Ipomoea asarifolia has a Pantropical distribution and is common in altered areas (Austin, & Cavalcante, 1982;Wood et al., 2020). In Brazil, it is widely distributed in the North and Northeast regions, in the Amazon, Caatinga and Atlantic Forest . Specimens examined: Nascimento, J.S. 4,5,7,15  6.10 Ipomoea ramosissima (Poir.) ChoisyFig. 3D. Habit: Herbaceous climber, twiner. Distribution: It occurs throughout tropical America, in sandbanks, forest edges, pastures, cultivated fields, and vacant lots . In Brazil, it occurs in all regions and phytogeographic domains (except in the Pantanal) . Specimens examined: Nascimento, J.S. 13 (HABIT). 7. Maripa Aubl. Maripa is represented by lianas reaching up to 40 m in height, with simple, generally coriaceous leaves, white, pink or purple corolla, simple or less frequently bifid style, globose stigma, and indehiscent and ligneous fruits (Austin, 1973;Pastore, 2020). This genus includes 20 species with distribution from Central America to northern South America, predominately in the Amazon Forest (Austin, 1973). Twelve species are recognized in Brazil, found in the North, part of the Midwest and the Northeast regions, in the Amazon and less frequently in Cerrado. Two species were reported for Maranhão (Pastore, 2020), and of the two species found in the Upper Turi-Gurupi region, one is a new record for Maranhão, thus raising to three the number of species known from the state.  (Austin, & Cavalcante, 1982). In Brazil, it occurs in the North and Northeast, restricted to the state of Maranhão in the latter, and it is an exclusively Amazonian species (Pastore, 2020 (Austin, & Cavalcante, 1982). In Brazil, it is recorded in the North and only in the state Mato Grosso in the Midwest, and it is an exclusively Amazonian species (Pastore, 2020). In this study, M. scandens is a new record for the state of Maranhão. Specimens examined: Pastore, M. 1499 (MG)

Odonellia K. R. Robertson
Odonellia is characterized by climbing habit, simple trichomes, simple leaves, glomeruliform or capituliform inflorescences, white corollas, sericeous midpetaline bands, entire style, globose stigma, and 4-valved capsules (Robertson, 1982). Odonellia has only two species, one of which is restricted to the Brazilian territory and the other is widely distributed from southern Mexico to northern South America (Robertson, 1982;Austin, & Cavalcante, 1982). Both species occur in Brazil and only one was registered for Maranhão by Simão-Bianchini (2020) and was found in the Upper Turi-Gurupi region in the present study.  (Robertson, 1982;Austin, & Cavalcante, 1982). In Brazil, the species occurs only in the Amazon and Cerrado (Simão-Bianchini, 2020). Specimens examined: Jangoux, I.J. 868 (RB)

Operculina Silva Manso
Operculina is characterized by climbing habit, angular or grooved usually winged petioles and pedicles, simple (entire or lobbed) or rarely compound leaves, sepals usually accrescent in fruit, white, yellow or reddened corollas with usually pubescent midpetaline bands, spirally twisted anthers after anthesis, entire styles, globose stigmas, and operculate capsules (Staples, Simões, & Austin, 2020). Operculina is distributed throughout the tropics of the world (Staples et al., 2020). Four species occur in Brazil, three in the Brazilian Amazon, and two in Maranhão .
In the Upper Turi-Gurupi region, it is represented by one species.
9.1 Operculina hamiltonii (G. Don) D.F. Austin, & Staples. Fig. 3N Habit: Herbaceous climber, twiner. Distribution: Southern Mexico, Central and South America (Staples et al., 2020). In Brazil, it occurs in all regions, except in the South, and in all phytogeographic domains, except Pampa . The great diversity of Ipomoea in the present study is due to the wide distribution and high richness of this genusthe largest of Convolvulaceaein the tropics and subtropics (Eserman et al., 2020). Conceição, Silva, and Rodrigues (2014) also indicated Ipomoea as the most representative genus in a survey of Convolvulaceae from a Cerrado fragment in Maranhão, demonstrating that the genus is diverse in the state.
In the Upper Turi-Gurupi region, I. asarifolia had the largest number (16%) of specimens in the survey. This species has a Pantropical distribution (Austin, & Cavalcante, 1982;Wood et al., 2020) and is common in altered areas. It was collected in large populations during this study, and presented a decumbent growth habit and large and showy flowers, often with intense pink-colored corollas (Figure 2A and B) and, less frequently, white corollas.
Color variation of the corollas from pink or lilac to white has been observed in some species of Convolvulaceae (Simão-Bianchini et al., 2016;Wood et al., 2020). Colors may vary even within the same individual. The color of the corolla is an important visual cue to attract pollinators, and variable color patterns can influence the frequency of visitation (Paz, 2011). It is also a key strategy when the species occur in environments with few floral visitors that act as potential pollinators or where pollination can be uncertain or occasional, such as in anthropized areas (Paz, 2011), as it is the case of environments where I. asarifolia occurs.
Most species found in this study have pink-to lilaccolored corollas with nectar guides, landing platforms, and nectariferous discs at the base of the ovary. Based on these attributes, these species can be classified as mellitophilous (Faegri, & van der Pijl, 1979). On the other hand, I. hederifolia and I. quamoclit, also included in this study, present red-colored hypocrateriform corollas, indicating pollination by hummingbirds (Streisfeld, & Rausher, 2009).
Most of the recorded species (15 spp.) have climbing habit, growing on plants, fences and other supporting structures, with Herbaceous, subwoody or woody branches. Only M. glabra and M. scandens have woody branches throughout their length, being lianas of larger size. Regarding the climbing mechanism, the voluble habit was found in the species studied here, bearing in mind that the climbing habit and the voluble mechanism are predominant in the family (Austin, 2015). The branches that wrap around a supporting structure normally present unidirectional growth (Hegarty, 1991;Vargas, Araújo, Schiavini, Rosa, & Hattori, 2013) and in the case of Convolvulaceae, the voluble branches are sinistrorse (Simão-Bianchini, & Pirani, 1997).
The other types of habits found in the species in this study were decumbent herb in I. asarifolia, I. batatas, and E. glomeratus; erect herb with decumbent branches in E. alsinoides; and erect shrub in I. carnea subsp. fistulosa.
Regarding the distribution of collections and species in the Upper Turi-Gurupi region, it is clear that despite the contribution of the present study, systematic collections of Convolvulaceae are still needed because much of the area remains unexplored (Figure 4).
Maripa scandens, found in this survey, is a new record for  (Esquivel-Muelbert et al., 2018) and anthropization processes such as deforestation and fires (Ferrante, & Fearnside, 2019) in the Amazon Forest of Maranhão. The number of collections and cataloged species reflects the few floristic studies conducted in the area over time. It is a consensus among researchers that the diversity of plants in the Amazon is undersampled: the current sampling density corresponds to ten collections per 100 km². There is, therefore, a void of information resulting from lack of collections and a shortage of taxonomists in certain botanical groups (Maldonado et al., 2015).
The little investment in collections in the Upper Turi-Gurupi region is a reflection of the low number of fragments suitable for botanical excursions, taking into account that only 17.6% of the total area of Amazon Forest in Maranhão lies within protected areas. These protected areas are two conservation unitsthe Baixada Maranhense Environmental Preservation Area and the Gurupi Biological Reserve (Silva, Rylands, & Fonseca, 2005;Almeida, & Vieira, 2010)and the Indigenous Lands integrating the so-called "Gurupi Mosaic" (Silva Junior et al., 2020). Despite being an integral protection conservation unit and one of the last protected remnants of Amazon Forest in the state of Maranhão, the Gurupi Biological Reserve has only 23% of primary forest preserved (Silva et al., 2005;Almeida, & Vieira, 2010). The vegetation in these legally protected areas is also degraded by fires and illegal logging, which had high rates registered between 2007 and 2019 (Silva Junior et al., 2020).
It is important to emphasize that the species were collected in Amazon Forest fragments that are under strong anthropogenic pressure, mainly due to deforestation, fires and agricultural activities. Such activities reduce the size of these fragments and affect the preservation of plant species. The fact that most species of Convolvulaceae sampled here are common in altered areas corroborate that a large part of the study area undergoes the impacts of deforestation and many fragments present anthropogenic influences and pioneer vegetation (Barbosa et al., 2007;Vital, 2009).

Conclusion
The results presented here contribute to increase the knowledge about the distribution and floristic diversity of Convolvulaceae in the Amazon region of Maranhão, since most of the studies published so far in the Northeast of Brazil were conducted in Caatinga and in the semiarid region. The record of a new Amazonian species for Maranhão in this survey and the observed sampling gap indicate that new records may still be documented and new species to science may still be described, highlighting the importance of this area for conservation. Moreover, the identification key and data about local species provided in the present study support future technical work for conservation and land use policies. The data obtained here encourage the conservation of the Amazonian flora of Maranhão since this area is under strong risk of environmental degradation and is one of the most threatened in terms of biodiversity loss in the Amazon domain, with continued devastation even within protected areas.