Epiphytic Lichens in Salt Flats as Biodiversity Refuges in Reserva Ecológica Arenillas

Abstract

The mangrove biome is a highly productive system globally, with flora and fauna adapted to significant saline influence, where salt flats coexist alongside these systems, emerging over sands and muds with high salinity and sparse vegetation. The objective of this research is to describe, for the first time in Ecuador, the diversity of epiphytic lichens in salt flats in the southern region of Ecuador. Two salt flats were selected where Avicennia germinans and Laguncularia racemosa were the dominant trees with the shrub Batis maritima. A total of 30 species of epiphytic lichens were recorded, with the families Arthoniaceae, Graphidaceae, and Ramalinaceae having the highest number of species, and crustose lichens with photobiont type Trentepohlia showed high richness. The salt flats in the southern region of Ecuador have a high richness of epiphytic lichen species, and the species composition is similar to mangroves, highlighting the importance of their conservation as biodiversity refuges for lichens and consequently other flora and fauna groups. Therefore, epiphytic lichens in salt flats can be used as model organisms to assess their conservation in tropical areas.

1. Introduction

The mangrove biome is a highly productive system on a global level [1,2,3]. Thus, these ecosystems are recognized as one of the most diverse and important ecosystems in the world [4,5], and provide the habitat and resources for a variety of flora and fauna species [6,7,8]. However, mangroves have been affected by significant human threats such as the overexploitation of forest resources, salt extraction, pollution, and land use changes [9,10,11,12]. One of the main threats is the shrimp industry, where ponds are constructed in salt flat areas for shrimp production that lack an environmental management system, leading to increasing pollution [13,14]. Among the great biodiversity of mangroves, less-studied groups such as lichens, bryophytes, bromeliads, and fungi are characteristic and diverse elements of these systems [8,15,16,17,18].

In this context, salt flats are ecosystems that coexist with mangroves and emerge over sands and muds, where the salt concentration in the soil is very high, sometimes showing sparse vegetation [19,20], but most studies have been conducted on mangroves rather than salt flats [21]. Nevertheless, lichens, also known as manglicolous lichens [8], have been previously studied in temperate zones [22,23,24] with limited studies in the Neotropics [25,26]. Additionally, in Ecuador, studies have only been conducted in the few localities of mangroves on the Galapagos Islands [27], and for continental Ecuador, studies have been carried out in dry forests [28]. However, although lichen specimens have been sampled from mangroves by researchers, more detailed and distributional studies based on systematic sampling have not been completed to date for the salt flats considered here, despite these areas being amongst the better-conserved salt flats areas of Ecuador.

Epiphytes are important organisms in mangroves [29], and the diversity and composition of the communities is determined by several factors related to the host tree traits (e.g., tree species, bark roughness, and tree size) and microclimatic factors [29,30,31,32,33]. Thus, we expect to find a higher diversity of epiphytic lichens in salt flats because they are ecosystems that coexist with mangroves. Studies on diversity in salt flats are scarce, describing a limited number of species, for example, in vascular plants [20,34], beetles [35], and microbial diversity [36]. For lichen diversity, there is a study where the genera of crustose Arthonia, Caloplaca, and Lecanora were registered [37]. Therefore, the objective of this research was to describe, for the first time in Ecuador, the diversity of epiphytic lichens in two salt flats of Reserva Ecológica Arenillas.

2. Materials and Methods

2.1. Study Area

This study was conducted in the salt flats of the Reserva Ecológica Arenillas, located in the province of El Oro in southern Ecuador (Figure 1). The area has a humid tropical climate in the coastal zone with temperatures ranging from 25 °C to 35 °C., with an area of 5791.85 km² (weather station Huaquillas for a recorded period of 45 years, 1969–2014).

2.2. Sampling Design and Data Collection

Two sampling areas were selected (Figure 2). Due to the complexity of the terrain in each salt flat, we randomly selected 20 host trees and shrubs. For each host, we recorded the presence or absence of epiphytic lichens. In both salt flats, the tree species Avicennia germinans and Laguncularia racemosa and the shrub Batis maritima were the most common. Additionally, herbaceous species such as Sporobolus pyramidatus, Sesuvium edmonstonei, S. portulacastrum, and Isocarpha microcephala were more abundant in both salt flats. Various published keys were used to identify the lichen specimens based on morphological, anatomical, and chemical characteristics. Traditional microscopy techniques were employed, along with spot tests using ultraviolet (UV) light, potassium hydroxide (K), commercial bleach (C), and Lugol’s solution (I). For lichen species’ nomenclature, we consulted MycoBank (www.mycobank.org, accessed on 8 February 2023) and the LIAS database (1995–2016), which provides a global information system for lichenized and non-lichenized ascomycetes (www.lias.net, accessed on 8 February 2023).

3. Results and Discussion

A total of 30 species were recorded in two salt flats, distributed in 15 genera and 10 families (

Table 1. Lichen species in salt flats. + = Species presence.

Specie	Family	Growth Form	Photobyont	Salt Flat 1	Salt Flat 2
Anisomeridium biforme	Monoblastiaceae	Crustose	Trentepohlia	+
Arthonia aff. conferta	Arthoniaceae	Crustose	Trentepohlia		+
Arthonia antillarum	Arthoniaceae	Crustose	Trentepohlia	+
Arthonia reniformis	Arthoniaceae	Crustose	Trentepohlia	+	+
Arthonia sp.	Arthoniaceae	Crustose	Trentepohlia	+
Bactrospora brevispora	Roccellaceae	Crustose	Trentepohlia	+	+
Bactrospora myriadea	Roccellaceae	Crustose	Trentepohlia		+
Çoniocarpon cinnabarinum	Arthoniaceae	Crustose	Trentepohlia	+	+
Dirinaria confluens	Caliciaceae	Foliose	Trebouxia	+
Dirinaria picta	Caliciaceae	Foliose	Trebouxia	+
Graphis anfractuosa	Graphidaceae	Crustose	Trentepohlia	+	+
Graphis leptospora	Graphidaceae	Crustose	Trentepohlia		+
Graphis sp. 1	Graphidaceae	Crustose	Trentepohlia	+
Graphis sp. 2	Graphidaceae	Crustose	Trentepohlia	+
Lecanora helva	Lecanoraceae	Crustose	Trebouxia		+
Lecanora leprosa	Lecanoraceae	Crustose	Trebouxia	+
Lecanora sp.	Lecanoraceae	Crustose	Trebouxia	+	+
Bacidia sp.	Ramalinaceae	Crustose	Trebouxia	+
Cratiria sp.	Caliciaceae	Crustose	Trebouxia	+
Opegrapha aff. diagrapha	Opegraphaceae	Crustose	Trentepohlia		+
Parmotrema aff. dominicanum	Parmeliaceae	Foliose	Trebouxia	+
Pyrenula cerina	Pyrenulaceae	Crustose	Trentepohlia	+	+
Pyrenula ochraceoflava	Pyrenulaceae	Crustose	Trentepohlia	+
Pyrenula sp. 1	Pyrenulaceae	Crustose	Trentepohlia	+
Pyxine petricola	Caliciaceae	Foliose	Trebouxia	+
Ramalina aff. darwiniana	Ramalinaceae	Fruticose	Trebouxia	+
Ramalina aspera	Ramalinaceae	Fruticose	Trebouxia	+
Ramalina complanata	Ramalinaceae	Fruticose	Trebouxia	+
Ramalina sideriza	Ramalinaceae	Fruticose	Trebouxia	+	+
Roccella gracilis	Roccellaceae	Fruticose	Trentepohlia	+	+

, Figure A1). The number of reported species is similar compared to the study by Sethy et al. [23] and Logesh et al. [22] in the mangroves of India, where 29 and 21 species of lichens were reported, respectively. However, it is higher than the 11 species of cyanolicens reported by Rangsiruji et al. [16] in the mangroves of Thailand and 19 species reported by Crespo and Atienza [37] in the salt flats of Spain.

The most representative families in these ecosystems are Arthoniaceae and Ramalinaceae with five species, followed by Graphidaceae with four species (Figure 3). These families are very numerous in dry ecosystems such as mangroves [22,23]. Additionally, Lücking et al. [38] describe, Graphidaceae with 2161 species, Ramalinaceae with 916 species, and Arthoniaceae with 717 species as among the most diverse families worldwide.

The most representative genus was Arthonia, where Crespo and Atienza [37] describe that Arthonia is very abundant in salt flats ecosystems of Spain. In our study, representative genera such as Dirinaria, Graphis, Lecanora, Pyrenula, Ramalina, and Rocella are very common in salt flats; similarly, previous studies indicate that these lichen genera are very characteristic in trees and shrubs with saline soils such as mangroves [8,22,23,24,25,26]. In addition, the genera Anisomeridium, Bactrospora, Opegrapha, Parmotrema, Ramalina, Roccella, and Pyxine were recorded for the first time in the studied salt flats.

Similarly, the growth type was dominated by crustaceous lichens with 21 species, followed by fruticose and foliose with 5 and 4 species, respectively (Figure 4). In agreement with our results in salt flats, crustose lichens are the most dominant in mangrove ecosystems [22,23,39]. Supporting our results, Benítez et al. [28] noted that 90% (110 species) of epiphytic lichens in the dry forests of the Reserva Ecológica Arenillas were crustaceous, followed by 11 and 1 species of foliose and fruticose lichens, respectively. In terms of foliose lichens, Rangsiruji et al. [16], shown the presence of 11 species in the study area, where the thallus foliose were abundant; however, the study is focused in cyanobacterial lichens.

In terms of species diversity in our study, Anisomeridium biforme, Arthonia antillarum, Arthonia aff. conferta, Coniocarpon cinnabarinum, Dirinaria confluens, Dirinaria picta, Pyrenula cerina, and Pyrenula ochraceoflava were reported. Similar to our findings in salt flats, other studies have also reported these species growing in mangroves [23,26,39,40,41]. Although our study reports the diversity of lichens in salt flats, other groups such as vascular plants, beetles, and bacteria [36,42,43] should be considered, as other countries have reported a high diversity of these organisms in these ecosystems.

Our findings suggest that salt flats serve as biodiversity refuges with high epiphytic lichen richness. However, other factors influencing lichen diversity in similar ecosystems, such as mangroves and dry forests, were not examined in this study. Variables such as topography, disturbance, forest type, microclimatic conditions (e.g., humidity, temperature, light), and host tree characteristics (e.g., species, bark type, pH, tree diameter) may influence epiphytic lichen diversity [8,28,44,45] in salt flats and should be investigated in future research.

4. Conclusions

The salt flats of the Reserva Ecológica Arenillas in southern Ecuador demonstrate a significant diversity of lichens, with 30 species. The growth type with the highest occurrence in salt flats was crustaceous, followed by fruticose and foliose lichens. This aligns with several studies in mangroves and dry forests, where crustose lichens were dominant. Therefore, epiphytic lichens in salt flats serve as valuable model organisms for evaluating conservation efforts in tropical mangroves, due to the fact that the species composition of salt flats are similar to mangroves. Additional sampling is necessary to explore environmental factors and their relationship with epiphytic lichens in these forests, as well as to gain a deeper understanding of lichen diversity in tropical salt flats.