Ecological Characterization of the Flora in Reserva Ecológica Arenillas, Ecuador

Abstract

Ecuador, located in the Neotropics, has 66 protected natural areas, which represent about 13.77% of its overall territory. The Reserva Ecológica Arenillas reserve (REAr), located in southwestern Ecuador, protects an area of dry forest, coastal thorn forest, and mangroves. This dry forest is part of the Pacific equatorial core and is included the Tumbes–Chocó–Magdalena, one of the 34 biodiversity hot spots of the world. It is an extremely fragile ecosystem and therefore the need for conservation is of the utmost importance. Knowledge of the flora and their ecological characteristics is still limited, which was one of the main objectives of this work. In this study, 118 plots located in different locations of the REAr were selected in order to sample the trees, shrubs, and herbaceous plants within them. This information was supplemented with data from the literature and the GBIF; life forms were included according to Raunkiaer’s classification and their growth habits. The flora of the REAr was represented by 381 species, belonging to 77 families. The two most numerous families were the Fabaceae (51 plant species) and Malvaceae (31 species). The dominant life form was the phanerophytes with 200 species (52.5%), followed by therophytes with 104 species (27.3%), and camephytes with 22 species (5.8%). Physiognomy was dominated by the herbaceous growth (44%). The biodiversity indices of two ecosystems were studied (The deciduous forest of the Jama-Zapotillo lowland and the low forest and deciduous shrubland of the Jama-Zapotillo lowland), obtaining higher values for the deciduous forest ecosystem of the Jama-Zapotillo lowland. With these indicators, a classification of each forest type was made by performing a hierarchical cluster analysis. The information provided in this paper is particularly important for focusing conservation efforts and preventing the loss of flora diversity in these forests, which are subject to great anthropogenic pressures.

1. Introduction

Ecuador is one of the 17 mega-diverse countries of the world [1]. It has 17,748 confirmed species of native flora, and it is estimated that with the continuation of studies of Ecuadorian flora, the total number of vascular plants could reach 25,000 species [2]. A large proportion of these species (1600) are included in the IUCN Red List. Furthermore, more species are added to the Red List every year. In 2019, a total of 354 new species were included in the list.

Dry ecosystems are one of the most valuable types of ecosystems in Ecuador. Together with dry ecosystems of northern Peru they form the Tumbesian Region. This is one of the areas of South America with the greatest number of endemic species, while at the same time being one of the most threatened regions [3]. Among the different dry ecosystems in the Tumbesian region in Ecuador, the equatorial dry forest is among the most fragile [4]. This is a unique ecosystem of the world and is located in the south of the country, in the regions of Esmeraldas, Manabí, Santa Elena, Guayas, El Oro, and Loja.

One of the main remnants of the equatorial dry forest in the south of Ecuador is the Reserva Ecológica Arenillas reserve (henceforth REAr). Moreover, it is the only ecological reserve that conserves mangroves and tropical dry forests in the southwestern region of the country. In spite of its ecological relevance, the REAr presents conservation problems, such as the fragmentation of its ecosystems, the expansion of agriculture and cattle ranching inside the limits of the reserve, and several climate change-related impacts [5]. Another difficulty encountered by the REAr is the redefinition of its limits. It has been a military base and an exclusion zone since the 1970s because of its strategic location on the border with Peru [6]. Originally, the former military base had an area of 22,000 ha. When the Ecological Reserve was created in 2001, the protected area comprised only 17,082.7 ha of the original extent and in 2012, it was reduced to 13,170.03 ha. [7].

Since the creation of the natural reserve, the REAr has been studied very little from a floristic point of view. One of the first studies was that of Ceron et al. [8], in which 105 species belonging to 49 families were identified. These results were similar to those found by Estrella and Troya [9] (104 species grouped into 82 genera and 48 families) and Ochoa et al. [10] (79 species grouped into 69 genera and 41 families). Nevertheless, other studies that were based on higher sampling efforts have documented highly diverse flora [11], indicating that increasing the sampling effort may reveal much larger numbers. Based on these studies and other studies in different dry forest regions, it is also known that there are evident differences in the composition and biodiversity between the different zones of the REAr [12], but the factors that delimit this special differentiation in the dry forest have not yet been explored in great detail. Thus, it becomes difficult to study and obtain rigorous conclusions about the current lists of scientific data on the species that exist in this ecosystem.

Overall, the REAr, due to its history, diversity of habitats, geographic location, and sociological environment, is an interesting biodiversity scenario for the study of conservation, monitoring of plant species, and the improvement of our knowledge of the main functions of this ecosystem that is threatened by anthropic pressure. However, not much information exists about its floral composition, diversity, and the underlying drivers. Therefore, the objective of this work was to analyze the floristic composition, ecological characteristics, and diversity of the ecosystems within the REAr. By doing so, we updated the information on the flora of the REAr, increasing its value for conservation initiatives and contributing to a proper design of future management and conservation actions.

2. Material and Methods

2.1. Study Area

This study is conducted in the REAr, which is located to the south of the equator between the cantons of Huaquillas and Arenillas (Figure 1), within the latitudes from 3°27′30.94″ S to 3°39′37.49″ S and from 80° 9′18.65″ W to 80° 9′47.93″ W. This reserve has an area of 13,170 ha and an average elevation of 120 m above sea level (masl) [8]. The REAr is composed of a matrix of dry forests, desert scrubs, and mangroves. The climate of the study area is warm-dry, with an average temperature of 24 °C, and rainfall varies between 300 and 500 mm/year from the lower elevated northern area of the reserve to the higher elevated southern part.

2.2. Characterization of the Richness, Composition, and Diversity of Flora Species in the REAr

According to the ecosystem classification system of Ecuador [13], we can find four types of ecosystems in the study area: (1) The deciduous forest of the Jama-Zapotillo lowland, (2) the low forest and deciduous shrubland of the Jama-Zapotillo lowland, (3) the mangrove of the Jama-Zapotillo, and (4) the low desert scrubs of the Jama-Zapotillo. In this study, we sampled 118 plots of 20 × 20 m surface areas in two of the different dry forest types (the low deciduous forest of the Jama-Zapotillo and low forest and deciduous shrubland of the Jama-Zapotillo) and in the mangrove (the mangrove of the Jama-Zapotillo) (Figure 1). Sampling locations were selected following a random design, but locations with difficult or impossible access were discarded. In each 20 × 20 m plot, four 5 × 5 m subplots were selected to study shrubs, and four 1 × 1 m subplots to study herbs. Life form classes were identified according to Raunkiaer’s classification [14]. Field sampling was carried out during the rainy season to achieve a better identification of the species, according to the flowering and fruiting times of most of the known species. The physiognomies of the plants (herbaceous, shrubs, and trees) were noted in the field during sampling. Each of the plots were georeferenced with a handheld GPS (GARMIN GPSMAP 65) with a 5 m horizontal accuracy. The list of flora of the REAr created by Molina Moreira in 2017 [11] was used as the basis for the study. This is the latest and most complete study conducted so far in the REAr, and included 291 species from 64 families. The specimens from this area that have already been deposited in the Reinaldo Espinoza Herbarium of the Universidad Nacional de Loja (LOJA), the Herbarium of the Universidad Técnica Particular de Loja (HUTPL), the Herbarium of the Universidad de Guayaquil (GUAY), and the Herbarium of the Universidad de Almería (HUAL) [15], were also studied.

A database was created with information on the species found in scientific literature and those detected during field sampling. This database was complemented with the records of the Global Biodiversity Information Facility (GBIF) [16] and Tropicos [17], and we used the information about the ecosystem type to locate where sampling plots or literature records were acquired according to the ecosystem classification system of continental Ecuador.

The nomenclature of the scientific names was based on Plants of the World Online, Kew Science (https://powo.science.kew.org/; last access on 15 August 2022), and the families were classified according to the APG IV classification system.

2.3. Data Analysis

Based on the field sampling records, we studied the plant diversity of the deciduous forest of the Jama-Zapotillo lowland and the low forest and deciduous shrubland of the Jama-Zapotillo lowland ecosystems. To achieve this, we selected the results of 110 plots (the remaining eight plots belonged to the mangrove ecosystem) and calculated species richness, abundance, and diversity. Species richness was calculated as the number of species present per plot. Abundance was calculated as the numbers of each individual species per plot. Two different diversity indices were used, Shannon’s index and Simpson’s index, according to Equations (1) and (2), respectively:

$$H=-\sum _{i=1}^S{p}_i x lo{g}_2 p_i$$

(1)

$$D=1-\sum {p_i}^2$$

(2)

where H = Shannon’s index, D = Simpson’s diversity index, pi = Abundance of specie i (N) relative to the total number of species (N), and S = species richness [18].

With these indicators obtained at the plot level in the two sampled ecosystems, a hierarchical cluster analysis was performed using Sorensen’s distance measure [19,20]. The Ward method was then used to achieve the highest clustering structure coefficient. The analysis was performed using the Agnes function of the cluster ‘factoextra’ package in the R software, version 4.2.1. [21].

This analysis was performed at the plot level and for each of the two sampled ecosystems within the REAr (the deciduous forest of the Jama-Zapotillo lowland and low forest and deciduous shrubland of the Jama-Zapotillo lowland), separately. Differences in the different indices between the classes obtained after hierarchical classification were tested by one-way ANOVA and HSD post hoc analyses using the ‘dplyr’ package of the R software version 4.2.1 [21]. The p-value was set to be <0.05.

We used the Ward method because of its strong grouping structure for our variables (abundance, richness, and diversity) (

Table 1. Agglomeration factors of the four clustering methods.

Deciduous Forest of the Jama-Zapotillo Lowland
Clustering Methods	Average	Single	Complete	Ward
Agglomeration factor	0.9491697	0.8425549	0.9721348	0.9872076
Low forest and deciduous shrubland of the Jama-Zapotillo lowland
Clustering methods	Average	Single	Complete	Ward
Agglomeration factor	0.8996283	0.7202592	0.9487867	0.9791087

).

3. Results

In the REAr, 381 plant species belonging to 77 families were identified. Physiognomy was dominated by the herbaceous growth form, containing 167 plant species (44%), followed by 134 species of shrubs (35%) and 80 species of trees (21%). The three largest families were the Fabaceae with 51 plant species, followed by the Malvaceae with 31 species and the Euphorbiaceae with 26 species. The dominant life forms were phanerophytes with 200 species (52.5%), followed by therophytes with 104 species (27.3%), chamephytes with 22 species (5.8%), epiphytes with 21 species (5.5%), hemicryptophytes with 21 species (5.5%), geophytes with 7 species (1.8%) and hydrophytes with 6 species (1.6%) (

Table 2. Summary of the list of vascular plants of the REAr, with their scientific name, family, growth habit, and life form, according to Raunkiaer’s classification (G, geophytes; H, hemicryptophytes; Hy, hydrophytes; P, phanerophytes; T, therophytes; E, epiphytes).

Family	Taxon	Life Form	Growth Habit
Acanthaceae	Dicliptera unguiculata Nees	T	Herb
Acanthaceae	Dicliptera peruviana (Lam.) Juss.	T	Herb
Acanthaceae	Dicliptera paposana Phil.	T	Herb
Acanthaceae	Dyschoriste repens (Nees) Kuntze	T	Herb
Acanthaceae	Justicia comata (L.) L.	T	Herb
Acanthaceae	Avicennia germinans (L.) L.	T	Herb
Acanthaceae	Ruellia floribunda Hook.	T	Herb
Acanthaceae	Ruellia blechum L.	T	Herb
Acanthaceae	Tetramerium nervosum Nees	T	Herb
Acanthaceae	Elytraria imbricata (Valh) Pers.	T	Herb
Achatocarpaceae	Achatocarpus pubescens C.H.Wright	P	Shrub
Aistroemeriaciae	Bomarea obovata Herb.	P	Herb
Aizoaceae	Trianthema portulacastrum L.	T	Herb
Aizoaceae	Sesuvium portulacastrum (L.) L.	T	Herb
Alismataceae	Echinodorus bracteatus Micheli	T	Herb
Amaranthaceae	Alternanthera echinocephala (Hook.f.) Christoph	T	Herb
Amaranthaceae	Alternanthera ficoidea (L.) P.Beauv.	T	Herb
Amaranthaceae	Alternanthera paronychioides A.St.-Hil.	T	Herb
Amaranthaceae	Alternanthera pubiflora (Benth.) Kuntze	T	Herb
Amaranthaceae	Alternanthera porrigens (Jacq.) Kuntze	T	Herb
Amaranthaceae	Alternanthera brasiliana (L) Kuntze	T	Herb
Amaranthaceae	Amaranthus polygonoides Roxb	T	Herb
Amaranthaceae	Iresine angustifolia Euphrasén	T	Herb
Amaranthaceae	Achyranthes aspera L.	T	Herb
Amaranthaceae	Iresine diffusa Humb. & Bonpl. ex Willd	T	Herb
Amaranthaceae	Chamissoa altissima (Jacq.) Kunth.	T	Herb
Amaranthaceae	Gomphrena holosericea (Mart.) Moq.	T	Herb
Amaranthaceae	Salicornia fruticosa (L.) L.	T	Herb
Amaryllidaceae	Leptochiton quitoensis (Herb.) Sealy	G	Herb
Amaryllidaceae	Eucrosia bicolor Ker Gaw	G	Herb
Anacardiaceae	Spondias mombin L.	P	Shrub
Anacardiaceae	Mangifera indica L.	P	Tree
Anacardiaceae	Loxopterygium huasango Spruce ex Engl	P	Tree
Apiaceae	Conium maculatum L.	T	Herb
Apocynaceae	Pseudomarsdenia cundurango (Rchb. f.) Schltr.	T	Herb
Apocynaceae	Prestonia mollis Kunth.	T	Herb
Apocynaceae	Asclepias L.	T	Herb
Apocynaceae	Asclepias L.	T	Herb
Apocynaceae	Asclepias curassavica L.	T	Herb
Apocynaceae	Rauvolfia littoralis Rusby	T	Herb
Apocynaceae	Rauvolfia tetraphylla L.	T	Herb
Apocynaceae	Cascabela thevetia (L) Lippold	P	Herb
Apocynaceae	Nerium oleander L.	P	Herb
Araceae	Anthurium barclayanum Engl.	H	Herb
Araceae	Anthurium soukupii Croat	H	Herb
Arecaceae	Saribus rotundifolius (Lam) Blume	P	Herb
Arecaceae	Adonidia merrillii (Becc) Becc.	P	Herb
Arecaceae	Pritchardia pacifica Seem & H.Wendl	P	Herb
Asparagaceae	Sansevieria trifasciata Prain	P	Herb
Asparagaceae	Yucca guatemalensis Baker	G	Shrub
Asteraceae	Acanthospermum microcarpum BLRob.	T	Herb
Asteraceae	Synedrella nodiflora (L) Gaertn.	T	Herb
Asteraceae	Emilia fosbergii Nicolson	T	Herb
Asteraceae	Eclipta prostrata (L.) L	T	Herb
Asteraceae	Viguiera dentata (Cav.) Spreng.	T	Herb
Asteraceae	Bidens pilosa L.	T	Herb
Asteraceae	Sphagneticola trilobata (L) Pruski	P	Shrub
Asteraceae	Tessaria integrifolia Ruiz & Pav.	P	Shrub
Asteraceae	Verbesina eggersii Hieron.	P	Shrub
Asteraceae	Verbesina lloensis Hieron	T	Shrub
Asteraceae	Barnadesia Mutis ex L.f.	T	Shrub
Asteraceae	Bidens bipinnata L.	T	Shrub
Asteraceae	Dasyphyllum Kunth	T	Herb
Asteraceae	Galinsoga Ruiz & Pav.	T	Herb
Asteraceae	Milleria quinqueflora L.	T	Herb
Asteraceae	Pseudogynoxys chenopodioides (Kunth) Cabrera	P	Shrub
Asteraceae	Tagetes erecta L.	T	Herb
Basellaceae	Anredera ramosa (Moq.) Eliasson	E	Herb
Bignoniaceae	Lundia Puerari ex DC.	T	Shrub
Bignoniaceae	Bignonia longiflora Cav.	P	Shrub
Bignoniaceae	Handroanthus billbergii (Bureau & K. Schum.) S.O.Grose	P	Tree
Bignoniaceae	Jacaranda mimosifolia D.Don	P	Tree
Bignoniaceae	Handroanthus chrysanthus (Jacq.) S.O.Grose	P	Tree
Bignoniaceae	Fridericia dichotoma (Jacq.)	P	Tree
Bignoniaceae	Mansoa hymenaea (DC.) A.H:Gentry	P	Tree
Bignoniaceae	Mansoa verrucifera (Schlecht) A.H.Gentry	P	Tree
Bignoniaceae	Tecoma castanifolia (D. Don.) Melch	P	Shrub
Bixaceae	Bixa orellana L.	P	Shrub
Bixaceae	Cochlospermum vitifolium (Willd.) Spreng	P	Tree
Boraginaceae	Cordia lutea Lam.	P	Shrub
Boraginaceae	Heliotropium angiospermum Murray	T	Shrub
Boraginaceae	Heliotropium curassavicum L.	T	Shrub
Boraginaceae	Heliotropium indicum L.	T	Shrub
Boraginaceae	Tournefortia microcalyx (Ruiz & Pav.) I.M.Johnst.	C	Shrub
Boraginaceae	Varronia cylindristachya Ruiz & Pav.	P	Shrub
Boraginaceae	Varronia macrocephala Desv.	P	Shrub
Bromeliaceae	Aechmea pyramidalis Benth.	H	Herb
Bromeliaceae	Bromelia pinguin L.	E	Herb
Bromeliaceae	Bromelia karatas L.	E	Herb
Bromeliaceae	Tillandsia multiflora Benth.	E	Herb
Bromeliaceae	Tillandsia usneoides (L.) L.	E	Herb
Bromeliaceae	Tillandsia streptocarpa Baker	E	Herb
Bromeliaceae	Tillandsia latifolia Meyen	E	Herb
Bromeliaceae	Tillandsia recurvata (Gaudich.) Baker	E	Herb
Bromeliaceae	Tillandsia triglochinoides C.Presl	E	Herb
Bromeliaceae	Tillandsia disticha Kunth.	E	Herb
Bromeliaceae	Tillandsia barclayana Baker.	E	Herb
Bromeliaceae	Tillandsia espinosae L. B. Sm.	E	Herb
Bromeliaceae	Tillandsia cyanea L. B. Sm.	E	Herb
Bromeliaceae	Tillandsia caerulea Kunth	E	Herb
Burseraceae	Bursera graveolens (Kunth) Triana & Planch	P	Tree
Cactaceae	Pilosocereus lanuginosus (L.) Byles & G:D. Rowley	P	Shrub
Cactaceae	Armatocereus cartwrightianus Backeb.	P	Shrub
Cactaceae	Armatocereus matucanensis Backeb.	P	Shrub
Cactaceae	Opuntia ficus-indica (L.) Mill.	P	Shrub
Cactaceae	Opuntia stricta (Haw) Haw.	P	Shrub
Cactaceae	Opuntia quitensis F.A.C. Weber	P	Shrub
Cactaceae	Melocactus peruvianus Vaupel	P	Shrub
Cactaceae	Selenicereus monacanthus (Lem) D.R.Hunt	P	Shrub
Cactaceae	Cereus hexagonus (L.) Mill.	P	Shrub
Cactaceae	Cephalocereus Pfeiff.	P	Shrub
Cactaceae	Cleistocactus Pfeiff.	P	Shrub
Cannabaceae	Celtis iguanaea (Jacq) Sarg	P	Shrub
Cannabaceae	Trema micrantha (L.) Blume	P	Shrub
Capparaceae	Beautempsia avicenniifolia Gaudich. ex Alleiz.	P	Shrub
Capparaceae	Capparicordis crotonoides (Kunth) Iltis & Cornejo	P	Shrub
Capparaceae	Colicodendron scabridum (Kunth)	P	Tree
Capparaceae	Cynophalla heterophylla (Ruiz & Pav. ex DC.) Iltis & Cornejo	P	Tree
Capparaceae	Cynophalla flexuosa (L.) J.Presl	P	Tree
Caricaceae	Carica papaya L.	P	Shrub
Caricaceae	Carica parviflora (A. DC.) Solms	P	Shrub
Celastraceae	Tricerma octogonum (L’Hér.) Lundell	P	Shrub
Combretaceae	Conocarpus erectus L.	P	Tree
Combretaceae	Terminalia catappa L.	P	Tree
Combretaceae	Laguncularia racemosa (L.) C.F.Gaertn	Hy	Tree
Commelinaceae	Commelina diffusa Burm.f.	P	Herb
Commelinaceae	Commelina Plum. ex L.	P	Herb
Commelinaceae	Calli cordifolia (Sw.) Andiers. & Woodson	P	Herb
Convolvulaceae	Camonea umbellata (L.) A.R.Simões & Staples	P	Herb
Convolvulaceae	Cuscuta acuta Engelm.	P	Herb
Convolvulaceae	Ipomoea batatas (L.) Lam.	P	Herb
Convolvulaceae	Evolvulus convolvuloides (Willd. ex Schult.) Stearn	T	Herb
Convolvulaceae	Evolvulus nummularius (L.) L.	T	Herb
Convolvulaceae	Ipomoea asarifolia (Desr.) Roem. & Schult.	T	Herb
Convolvulaceae	Ipomoea cholulensis Kunth	P	Herb
Convolvulaceae	Ipomoea hederifolia L.	T	Herb
Convolvulaceae	Ipomoea regnellii Meisn.	P	Herb
Convolvulaceae	Ipomoea quamoclit L.	P	Herb
Convolvulaceae	Ipomoea pes-caprae (L.) R. Br.	P	Herb
Convolvulaceae	Ipomoea nil (L) Roth	P	Herb
Convolvulaceae	Ipomoea carnea Jacq.	P	Herb
Convolvulaceae	Ipomoea triloba Thunb	P	Herb
Convolvulaceae	Jacquemontia corymbulosa Benth	P	Herb
Convolvulaceae	Jacquemontia unilateralis (Roem. & Schult.) O’Donell	P	Herb
Convolvulaceae	Distimake aegyptius (L.) A.R.Simões & Staples	P	Herb
Cucurbitaceae	Momordica charantia L.	P	Herb
Cucurbitaceae	Luffa operculata (L.) Cogn.	P	Herb
Cucurbitaceae	Cucurbita pepo L.	T	Herb
Cucurbitaceae	Cayaponia glandulosa (Mart.) Cogn.	T	Herb
Cucurbitaceae	Echinopepon racemosus (Steud.) C. Jeffrey	P	Herb
Cyperaceae	Cyperus squarrosus L.	H	Herb
Cyperaceae	Cyperus compressus L.	H	Herb
Cyperaceae	Cyperus ligularis L.	H	Herb
Cyperaceae	Cyperus microbolbos C.B.Clarke	H	Herb
Cyperaceae	Fimbristylis littoralis Gaudich.	Hy	Herb
Erythroxylaceae	Erythroxylum glaucum O. E. Schulz	P	Herb
Erythroxylaceae	Erythroxylum acuminatum Ruiz & Pav.	P	Shrub
Euphorbiaceae	Jatropha curcas L.	P	Shrub
Euphorbiaceae	Euphorbia serpens Kunth.	T	Shrub
Euphorbiaceae	Euphorbia hirta L.	T	Shrub
Euphorbiaceae	Euphorbia heterophylla L.	T	Shrub
Euphorbiaceae	Cnidoscolus aconitifolius (Mill.) IM Johnst.	P	Shrub
Euphorbiaceae	Croton hirtus L’Hér.	P	Shrub
Euphorbiaceae	Croton fraseri Mull. Arg.	P	Shrub
Euphorbiaceae	Croton rivinifolius Kunth	P	Shrub
Euphorbiaceae	Croton eggersii Pax	P	Shrub
Euphorbiaceae	Croton aequatoris Croizat	P	Shrub
Euphorbiaceae	Croton eggersii Pax	P	Shrub
Euphorbiaceae	Croton jamesonii Müll. Arg.	P	Shrub
Euphorbiaceae	Croton schiedeanus Schltdl.	P	Shrub
Euphorbiaceae	Codiaeum variegatum (L.) Rumph. ex A.Juss	P	Shrub
Euphorbiaceae	Acalypha villosa Jacq.	P	Shrub
Euphorbiaceae	Acalypha subcastrata F.Aresch.	T	Shrub
Euphorbiaceae	Acalypha diversifolia Jacq.	P	Shrub
Euphorbiaceae	Acalypha cuspidata Jacq.	P	Shrub
Euphorbiaceae	Acalypha setosa A. Rich.	P	Shrub
Euphorbiaceae	Acalypha cuspidata Jacq.	P	Shrub
Euphorbiaceae	Acalypha alopecuroides L.	T	Shrub
Euphorbiaceae	Dalechampia scandens L.	T	Shrub
Euphorbiaceae	Codiaeum variegatum (L.) Rumph. ex A. Juss.	P	Shrub
Euphorbiaceae	Manihot esculenta Crantz	G	Tree
Fabaceae	Senegalia polyphylla (DC.) Britton & Rose	P	Tree
Fabaceae	Vachellia macracantha (Humb. & Bonpl. ex Willd.) Seigler & Ebinger	P	Tree
Fabaceae	Aeschynomene tumbezensis J.F. Macbr.	P	Tree
Fabaceae	Aeschynomene scoparia Kunth	P	Tree
Fabaceae	Aeschynomene americana L.	T	Tree
Fabaceae	Albizia multiflora (Kunth) Barneby y J.W.Grimes	P	Tree
Fabaceae	Caesalpinia pulcherrima (L.) Sw.	P	Tree
Fabaceae	Chloroleucon mangense (Jack.) Britton & Rose	P	Tree
Fabaceae	Calliandra tumbeziana J.F. Macbr.	T	Shrub
Fabaceae	Canavalia ensiformis (L.) DC.	T	Shrub
Fabaceae	Canavalia rosea (SW)	P	Shrub
Fabaceae	Canavalia brasiliensis Mart. ex Benth.	P	Shrub
Fabaceae	Centrosema pubescens Benth.	P	Shrub
Fabaceae	Cercidium praecox (Ruiz & Pav) Hawkins	P	Shrub
Fabaceae	Chamaecrista nictitans (L.) Moench	T	Shrub
Fabaceae	Crotalaria incana L.	P	Herb
Fabaceae	Coursetia caribaea Ochroleuca (Jacq.)	P	Shrub
Fabaceae	Delonix regia (Bojer ex Hook.) Raf.	P	Tree
Fabaceae	Desmanthus virgatus (L.) Willd.	T	Herb
Fabaceae	Desmodium scorpiurus (Sw.) Desv. ex DC.	T	Shrub
Fabaceae	Desmodium procumbens (Mill.) C.L.Hitchc.	T	Shrub
Fabaceae	Erythrina smithiana Krukoff	P	Tree
Fabaceae	Erythrina velutina Willd.	P	Tree
Fabaceae	Geoffroea spinosa Jacq.	P	Tree
Fabaceae	Indigofera subulata Vahl ex Poir.	P	Tree
Fabaceae	Leucaena trichodes (Jacq.) Benth.	P	Tree
Fabaceae	Libidibia glabrata (Kunth) C.Cast. & G.P.Lewis	P	Tree
Fabaceae	Machaerium Pers.	P	Tree
Fabaceae	Machaerium millei Standl.	P	Tree
Fabaceae	Mimosa albida Humb. & Bonpl. ex Willd	P	Tree
Fabaceae	Mimosa acantholoba (Humb. & Bonpl. ex Willd.) Poir.	P	Tree
Fabaceae	Mimosa pigra L.	P	Tree
Fabaceae	Neptunia plena (L.) Benth.	T	Shrub
Fabaceae	Parkinsonia aculeata L.	P	Tree
Fabaceae	Pithecellobium dulce (Roxb.) Benth.	P	Tree
Fabaceae	Piptadenia retusa (Jacq.) P.G.Ribeiro, Seigler & Ebinger	P	Tree
Fabaceae	Piscidia carthagenensis Jacq.	P	Tree
Fabaceae	Pithecellobium excelsum (Kunth) Mart.	P	Tree
Fabaceae	Prosopis juliflora (Sw.) DC.	P	Tree
Fabaceae	Prosopis pallida (Willd.) (Humb. & Bonpl. ex Willd.) Kunth	P	Tree
Fabaceae	Phaseolus vulgaris L.	T	Herb
Fabaceae	Pseudosamanea guachapele (Kunth) Harms	P	Tree
Fabaceae	Samanea saman (Jacq.) Merr.	P	Tree
Fabaceae	Senna mollissima (Humb. & Bonpl. ex Willd.) H.S.Irwin & Barneby	P	Tree
Fabaceae	Senna oxyphylla (Kunth) H.S.Irwin & Barneby	P	Tree
Fabaceae	Galactia striata (Jacq.) Urb.	P	Herb
Fabaceae	Vigna caracalla (L.) Verdc.	T	Herb
Fabaceae	Schizolobium parahyba (Vell.) S.F. Blake	P	Tree
Fabaceae	Stylosanthes scabra Vogel	P	Herb
Fabaceae	Stylosanthes guianensis (Aubl.) Sw.	P	Herb
Fabaceae	Inga edulis Mart.	P	Tree
Lamiaceae	Hyptis atrorubens Poit.	T	Shrub
Lamiaceae	Tectona grandis L. f.	P	Tree
Loasaceae	Gronovia scandens L.	P	Herb
Loasaceae	Mentzelia aspera L.	T	Herb
Loranthacea	Psittacanthus divaricatus (Kunth) G.Don	P	Shrub
Lythraceae	Adenaria floribunda Kunth	P	Shrub
Malpighiaceae	Bunchosia plowmanii W.R. Anderson	P	Shrub
Malpighiaceae	Malpighia glabra L.	P	Shrub
Malpighiaceae	Malpighia emarginata DC.	P	Shrub
Malvaceae	Abutilon pedunculare Kunth	P	Shrub
Malvaceae	Abutilon reflexum (Lam.) Sweet	P	Shrub
Malvaceae	Abutilon umbellatum (L.) Sweet	P	Shrub
Malvaceae	Abutilon dianthum C. Presl	P	Shrub
Malvaceae	Ayenia magna L.	P	Shrub
Malvaceae	Bastardia bivalvis (Cav.) Kunth ex Griseb.	P	Shrub
Malvaceae	Bastardia viscosa (L.) Kunth	P	Shrub
Malvaceae	Ceiba trichistandra (A. Gray) Bakh.	P	Tree
Malvaceae	Cienfuegosia tripartita (Kunth) Gürke	T	Herb
Malvaceae	Corchorus orinocensis Kunth	T	Shrub
Malvaceae	Eriotheca ruizii (K. Schum.) A. Robyns	P	Tree
Malvaceae	Guazuma ulmifolia Lam.	P	Tree
Malvaceae	Hibiscus escobariae Fryxell	P	Shrub
Malvaceae	Hibiscus phoeniceus Jacq.	P	Shrub
Malvaceae	Hibiscus rosa-sinensis L.	P	Shrub
Malvaceae	Hibiscus pernambucensis Arruda	P	Shrub
Malvaceae	Malachra fasciata Jacq.	T	Shrub
Malvaceae	Malvaviscus concinnus Kunth	P	Shrub
Malvaceae	Byttneria parviflora Benth.	C	Shrub
Malvaceae	Byttneria glabrescens Benth.	C	Shrub
Malvaceae	Gaya peruviana Ulbr. f.	C	Shrub
Malvaceae	Sida acuta Burm.f.	C	Shrub
Malvaceae	Sida ciliaris L.	C	Herb
Malvaceae	Sida repens Dombey ex Cav.	C	Herb
Malvaceae	Sida setosa Mart. ex Colla	C	Herb
Malvaceae	Theobroma cacao L.	P	Shrub
Malvaceae	Wissadula diffusa R.E.Fr.	C	Shrub
Malvaceae	Pavonia fruticosa (Mill.) Fawc. &Rendle	C	Shrub
Malvaceae	Triumfetta bogotensis DC.	C	Shrub
Malvaceae	Gossypium barbadense L.	P	Shrub
Malvaceae	Sidastrum paniculatum (L.) Fryxell	T	Shrub
Marantaceae	Thalia geniculata L.	T	Shrub
Meliaceae	Cedrela odorata L.	P	Tree
Meliaceae	Azadirachta indica A. Juss.	P	Tree
Moraceae	Ficus citrifolia Mill.	P	Tree
Moraceae	Ficus elastica Roxb. ex Hornem.	P	Tree
Moraceae	Artocarpus altilis (Parkinson) Fosberg	P	Shrub
Moringaceae	Moringa oleifera Lam.	P	Tree
Muntingiaceae	Muntingia calabura L.	P	Herb
Musaceae	Musa x paradisiaca L.	T	Herb
Myrtaceae	Eugenia biflora (L.) DC.	P	Herb
Nyctaginaceae	Boerhavia coccinea Mill.	T	Herb
Nyctaginaceae	Boerhavia erecta L.	T	Shrub
Nyctaginaceae	Pisonia floribunda Hook. f.	P	Shrub
Nyctaginaceae	Pisonia ambigua Heimerl	P	Shrub
Nyctaginaceae	Pisonia aculeata L.	P	Shrub
Nyctaginaceae	Bougainvillea peruviana Bonpl	P	Shrub
Nyctaginaceae	Bougainvillea spectabilis Willd.	P	Shrub
Nyctaginaceae	Cryptocarpus pyriformis Kunth	P	Herb
Nyctaginaceae	Mirabilis violacea (L.) Heimerl	T	Herb
Nyctaginaceae	Mirabilis nyctaginea (Michx.) MacMill.	T	Herb
Nymphaeaceae	Nymphaea ampla (Salisb.) DC.	Hy	Herb
Nymphaeaceae	Nymphaea pulchella DC.	Hy	Tree
Oleaceae	Priogymnanthus apertus (B.Ståhl) P.S.Green	P	Shrub
Onagraceae	Ludwigia linifolia (Vahl) R.S.Rao	T	Shrub
Onagraceae	Ludwigia octovalvis (Jacq.) P.H. Raven	T	Shrub
Opilaceae	Agonandra excelsa Griseb.	P	Herb
Orchidaceae	Oncidium hyphaematicum Rchb.f	E	Herb
Orchidaceae	Epidendrum bracteolatum C. Presl	E	Herb
Orchidaceae	Notylia replicata Rchb.f.	E	Herb
Orchidaceae	Rodriguezia strobelii Garay	E	Herb
Orchidaceae	Zelenkoa onusta (Lindl.) M.W.Chase & N.H.Williams	E	Herb
Orchidaceae	Encyclia aspera (Lindl.) Schltr	E	Herb
Orchidaceae	Campylocentrum micranthum (Lindl.) Rolfe	E	Herb
Oxalidaceae	Oxalis dombeyi A.St.-Hil.	G	Herb
Oxalidaceae	Oxalis microcarpa Benth.	G	Herb
Passifloraceae	Passiflora biflora Lam.	P	Herb
Passifloraceae	Passiflora eggersii Harms	P	Herb
Passifloraceae	Passiflora suberosa L.	P	Herb
Phyllanthaceae	Phyllanthus niruri L.	T	Shrub
Phytolaccaceae	Achatocarpus pubescens C.H.Wright	P	Tree
Piperaceae	Peperomia pellucida (L.) Kunth	T	Herb
Plumbaginaceae	Plumbago scandens L.	T	Herb
Poaceae	Cynodon dactylon (L) Per.	H	Herb
Poaceae	Echinochloa colonum (L.) Link	H	Herb
Poaceae	Lasiacis divaricata (L.) Hitchc	H	Herb
Poaceae	Paspalum vaginatum Sw.	H	Herb
Poaceae	Sporobolus pyramidatus (Lam.) Hitchc.	H	Herb
Poaceae	Panicum trichoides Sw.	H	Herb
Poaceae	Panicum polygonatum Schrad.	H	Herb
Poaceae	Panicum maximum (Jacq.)	H	Herb
Poaceae	Olyra latifolia L.	H	Herb
Poaceae	Setaria palmifolia (J. Koenig) Stapf	H	Herb
Poaceae	Chloris virgata Sw.	H	Herb
Polygalaceae	Asemeia violacea (Aubl.) J.F.B.Pastore & J.R.Abbott	T	Herb
Polygalaceae	Polygala paniculata L.	T	Herb
Polygonaceae	Triplaris cumingiana Fisch. & C.A. Mey.	P	Tree
Polygonaceae	Coccoloba ruiziana Lindau	P	Tree
Portulacaceae	Portulaca oleracea L.	H	Herb
Primulaceae	Bonellia sprucei (Mez) B.Ståhl & Källersjö	P	Tree
Pteridaceae	Adiantum raddianum C. Presl	G	Herb
Pteridaceae	Acrostichum aureum L.	H	Herb
Rhamnaceae	Scutia spicata (Humb. & Bonpl. ex Schult.) Weberb.	C	Tree
Rhamnaceae	Gouania mollis Reissek	C	Tree
Rhamnaceae	Sarcomphalus thyrsiflorus (Benth.) Hauenschild	P	Tree
Rhizophoraceae	Rhizophora × harrisonii Leechm.	Hy	Tree
Rhizophoraceae	Rhizophora mangle L.	Hy	Tree
Rubiaceae	Simira ecuadorensis (Standl.) Steyerm.	P	Tree
Rubiaceae	Randia armata (SW.) DC.	P	Shrub
Rubiaceae	Sphinctanthus aurantiacus (Standl.) Fagerl.	P	Shrub
Rubiaceae	Ixora coccinea L.	P	Shrub
Rubiaceae	Sommera purdiei Standl.	P	Shrub
Rubiaceae	Duroia hirsuta (Poepp.) K.Schum.	P	Tree
Rubiaceae	Spermacoce remota Lam.	P	Tree
Rubiaceae	Morinda citrifolia L.	P	Tree
Rutaceae	Zanthoxylum martinicense (Lam.) DC.	P	Tree
Rutaceae	Zanthoxylum rigidum Humb. & Bonpl. ex Willd.	P	Tree
Rutaceae	Amyris balsamifera L.	P	Shrub
Rutaceae	Citrus ×sinensis (L.) Osbeck	P	Tree
Rutaceae	Citrus × limon (L.) Osbeck	P	Tree
Rutaceae	Zanthoxylum fagara (L.) Sarg.	P	Tree
Sapindaceae	Sapindus saponaria L.	P	Tree
Sapindaceae	Serjania mucronulata Radlk.	P	Shrub
Sapindaceae	Cardiospermum corindum L.	P	Herb
Scrophulariaceae	Capraria peruviana Benth	C	Shrub
Solanaceae	Solanum peruvianum L.	T	Herb
Solanaceae	Browallia americana L.	T	Herb
Solanaceae	Solanum filiforme Ruiz & Pav.	T	Herb
Solanaceae	Solanum nigrum L.	T	Herb
Solanaceae	Solanum pimpinellifolium L.	T	Herb
Solanaceae	Lycianthes ecuadorensis Bitter	T	Herb
Solanaceae	Lycianthes cyathocalyx (Van Heurck & Müll. Arg.) Bitter	T	Herb
Solanaceae	Witheringia solanacea L’He’r	C	Herb
Solanaceae	Lycium nodosum Jacq.	P	Herb
Solanaceae	Capsicum annuum L.	C	Herb
Talinaceae	Talinum paniculatum (Jacq.) Gaertn.	H	Shrub
Talinaceae	Talinum fruticosum (L.) Juss.	T	Shrub
Tropaeolaceae	Tropaeolum harlingii Sparre	P	Shrub
Urticaceae	Laportea aestuans (L.) Chew	T	Shrub
Verbenaceae	Citharexylum quitense Spreng.	T	Tree
Verbenaceae	Citharexylum gentryi Moldenke	T	Tree
Verbenaceae	Lantana sprucei Hayek	C	Shrub
Verbenaceae	Lantana fucata Lindl.	C	Shrub
Verbenaceae	Lantana camara L.	C	Shrub
Verbenaceae	Lantana trifolia L.	C	Shrub
Verbenaceae	Lantana verticillata verticillata (L.) Nicolson	P	Herb
Verbenaceae	Lantana velutina M. Martens & Galeotti	C	Shrub
Verbenaceae	Lantana horrida Kunth	C	Shrub
Vitaceae	Cissus erosa Rich.	P	Herb
Zygophyllaceae	Kallstroemia pubescens (G.Don) Dandy	T	Herb

).

Forest Classification

Based on the hierarchical grouping performed on the similarities of species richness, abundance, Shannon index, and Simpson index (Supplement S1 in Supplementary Material), we identified three dry forest types in the deciduous forest of the Jama-Zapotillo lowlands ecosystem. Type I (black line) contains 12 sample plots, type II (red line) contains 26 sample plots and type III (green line) contains 19 sample plots (Figure 2).

The mean values of the diversity indices showed significant differences between forest types I and III. Type I presented the highest species richness (6.16) and abundance (18.58). The type I forest was also the ecosystem with the highest values of the two different diversity indices, but no significant differences were found between this ecosystem and ecosystem type III. Forest type III had the lowest values of both diversity indices. The highest values of richness, abundance, and diversity that were found in forest type I (Figure 3) fits with the specific features that define a conserved forest, with some relevant species such as Handroanthus chrysanthus, Eriotheca ruizii, Bursera graveolens, and Ceiba trischistandra. The maximum height that was determined in this forest was 27 m, which was represented by the presence of the species Ceiba trischistandra.

As similarly observed in the deciduous forest of the Jama-Zapotillo lowland, the hierarchical grouping of the low forest and deciduous shrubland of the Jama-Zapotillo lowland discriminated three forest types based on the similarity of the indicators: species richness, abundance, Shannon index, and Simpson index. Type I (black line) contains 27 plots, type II (red line) contains 5 plots and type III (green line) 21 plots. (Figure 4).

Significant differences in species richness (p-value = 1.27 × 10⁻⁶), abundance (p-value < 2 × 10⁻¹⁶), and Shannon index (p-value = 0.00712) were identified among the three forest types identified for this ecosystem. Forest type III had the highest species richness (7.00), abundance (20.20), alpha diversity with Simpson’s index (0.72), and Shannon index (1.63), which represent characteristics that define a well preserved forest (Figure 5). In type III, the following species stood out: Cochlospermum vitifolium, Handroanthus chrysanthus, Caesalpinia glabrata, and Geoffroea spinosa. The maximum height that was determined in this forest was 13 m.

4. Discussion

The detailed floristic analysis of our study reveals that, despite only focusing our sampling on two of the four ecosystems, [13], the richness and diversity of the species in this ecological reserve is greater than what was described in the last catalog of vascular flora detailing the complete sets of ecosystems included within the REAr [11]. The physiognomy of the species found in the study area was dominated by the herbaceous growth form with 167 species (44%). This is particularly interesting, as the tree species component in the tropical dry forests of the equatorial Pacific region is known, but knowledge of the shrubs and herbs is very limited. Nevertheless, seasonal dry forests have a very wide range of climatic tolerance [22], the predominance of herbaceous species over tree species may be due to the climatic conditions [23,24,25]. In the present study, all flora species were inventoried during the rainy season, corresponding with the onset of herbaceous flora.

Our findings are similar to those obtained in studies analyzing the floristic features of the dry forests of the central coastal Andes mountains that cover the Tumbesian region (58 forest families) [24] and other studies on Ecuador’s dry forests that report data on woody plant species [26,27]. Among all of the families, the Fabaceae was the most abundant, followed by the Malvaceae and Euphorbiaceae, and the dominant species in the reserve was the Handroanthus chrysanthus. These results are in accordance with previous studies reporting the Fabaceae as the best represented group in neotropical dry forests [28] and with specific studies in this region. For example, Molina [11] documented that the Fabaceae and Euphorbiaceae were the two predominant families in the REAr, and Luna et al. [12] cited the Fabaceae and Malvaceae as the most representative families. In 2006, Cerón et al. [8] reported that the Malvaceae and Poaceae were the most numerous families, with 8 species each, while the Fabaceae had 7 species.

Species assemblages in tropical dry forests appear to be primarily controlled by altitude and water availability [28], and the life forms reflect the bioclimate of the area. Raunkiaer [14] designed three main phytoclimates based on the landform spectrum, including phanerophyte for the tropics, therophyte for xeric environments, and hemicryptophyte for the cool temperate region. The present study identified seven different classes of life forms in the study area. As is the case in most dry forest remnants, our study reveals that the dominant life forms in the REAr were phanerophytes (52.5%) and terophytes (86%).

Many botanists have collected and studied the flora of Ecuador since the early 18th century [29,30,31,32]; the findings of our study highlight the importance of conserving the forests of the REAr and the species composition of the region. The analysis of species dominance and diversity within the REAr shows that 35% of the tree species identified are exclusive to the large floristic group of the Central Andes of the neotropical dry forest coast [24]. In the seasonal dry forests of Ecuador and Peru, 313 woody species can be found [33]. The presence of the Andes is one of the main causes of the isolation of the trans-Andean Pacific coastal region, which is characterized by the high levels of floristic endemism in the seasonal dry forests of Ecuador [33,34].

Many species are shared between dry forest formations and between the provinces of Ecuador [26]. In this study, we have observed that the species richness and diversity of REAr ecosystems depend on the dominant ecosystem type. Herbaceous species abundance and Shannon type diversity were higher in the deciduous forest of the Jama-Zapotillo lowland. The dominant families by number of species, density, abundance, and dominance of individuals are: the Fabaceae, Mimosaceae, Moraceae, and Bombacaceae [35,36]. The species composition analysis of this dry forest was dominated by species such as Handroanthus chrysanthus and revealed a general pattern of variation in community diversity and species composition. Several authors [26,34,37] have reported similar composition patterns of this species in the dry forests of the same region. The dendrograms divide the ecosystems studied into three types that differ in richness, abundance, and diversity. This seems to be related to the anthropic pressures exerted, with the least rich and diverse areas being the most degraded near the border, roads, or agricultural environments.

The information provided in this study is especially relevant due to the fragility of the tropical dry forest, which is the main ecosystem within the REAr and is the ecosystem where our specific data collection has been performed. Indeed, the tropical dry forest is one of the most threatened biomes in the world [26,38] and has experienced one of the most extensive rates of habitat loss during the last few decades [38]. Be that as it may, it is a much less-studied ecosystem than other tropical ecosystems, such as rainforests [6]. The small extension and high fragmentation of the Ecuadorian dry forests makes them more sensitive than those which are located in other countries [39]; this situation is especially relevant in the REAr. Despite being classified as a natural reserve, the highest protection level in Ecuador, it is a vulnerable area due to the constant pressure of extracting resources and expanding the agricultural and ranching areas within the REAr limits. In addition, clandestine crossings by outsiders and the deforestation of trees to create new access routes occur in this border area. These activities exert a strong negative impact on the vegetation. Further studies are needed on the biodiversity of the REAr and the relationships within the ecosystems and external pressures. Furthermore, transdisciplinary initiatives that take into account the ecological and human dimensions are a priority for safeguarding the integrity of the REAr [40,41] along with similar regions. Strategies can be implemented in this manner to reduce the negative impacts on these regions and provide alternative livelihoods for local communities. This would allow for the sustainable use and conservation of the REAr’s invaluable biodiversity for future generations, as well as its associated ecosystem services [42,43,44].

5. Conclusions

The present study reveals that the REAr has a greater floristic diversity than has previously been described. These new data are beneficial for the protection and conservation of this region.

The predominant life forms are phanerophytes and terophytes, which are conditioned by the presence of dry tropical climate in deciduous forests.

Within the dry forest zone, there is a great variety of forest types with different levels of richness, possibly because of differences in the level anthropogenic pressure between zones (i.e., greater impacts and more degraded areas with less richness are on the edges of the reserve, the areas closest to access roads or agricultural zones).