Updated List of Bryophytes from Cape Verde Archipelago

Abstract

The aim of the present study is to update the list of bryophytes in the Cape Verde archipelago, with a focus on its distinctive terrestrial biota. The research was carried out through a combination of herbarium collections revision and fieldwork conducted from 2016 to 2019. The revised list includes 185 bryophyte taxa (175 species, 5 subspecies, and 5 varieties) from 93 genera and 42 families. Notably, 8 taxa are endemic, and the inclusion of 35 new taxa further enriches the bryophyte diversity of the archipelago. The distribution of bryophyte taxa varies across islands, with Santo Antão, São Nicolau, and Fogo exhibiting particularly high diversity. Acrocarpous mosses are the most common growth form (58.4%), followed by pleurocarpous mosses, thalloid liverworts (15.1% each), and leafy liverworts (11.4%). In conclusion, this study provides valuable insights into the bryophyte diversity of southern Macaronesia enhancing our understanding of its unique flora and emphasizing the imperative need for conservation efforts.

1. Introduction

Oceanic islands are characterized by unique terrestrial biota with high proportions of endemic species that evolved in isolation from continental areas. The unique biota that makes island biodiversity special also leaves it particularly vulnerable to anthropogenic threats, such as invasive species, land use, and global warming.

In Europe, the Macaronesia archipelagos stand out as a hotspot of biodiversity with high numbers of endemic plant species [1]. The early land plant lineages, including bryophytes (liverworts, mosses, and hornworts), diversified less than vascular plants in Macaronesia. However, especially the northern Macaronesian archipelagos (Azores, Canaries, Madeira) still harbor a high bryophyte diversity that plays a vital role in ecosystem functioning [2]. The approximately 750 bryophyte taxa (including 56 endemics) of the northern Macaronesian islands correspond to ca. 40% of the European bryophyte species richness [3]. The southern Macaronesian Cape Verde archipelago harbors high botanical diversity as well [4]. During the past 15 years, there has been an impressive increase in the understanding of phylogenetic and phylogeographic relationships of bryophytes in northern Macaronesia. Although Laurisilva vegetation is absent [5], the Cape Verde islands provide an important refuge for vascular plants and bryophytes, particularly in communities at higher elevations. Furthermore, Cape Verde stands out due to its mixture of representatives of Afrotropical, Neotropical, Mediterranean, and Asian elements [6]. Comparisons of total bryophyte flora indicated the closest relationships with Sub-Saharan Africa and clear separation from the northern Macaronesian archipelagos [7].

The first Cape Verde list published by Patiño and González-Mancebo [8] enumerates 153 bryophyte taxa comprising 37 liverworts and hornworts and 116 mosses. More recent work by Garcia et al. [9] refers to approximately 185 taxa, including 7 endemics, and Martins et al. [10] add a new endemic to Cape Verde. However, further fieldwork and taxonomic revision of herbarium bryophyte material from Cape Verde enable us to clarify the total number of taxa for the archipelago. The aim of the present study was to update the list of bryophytes from Cabo Verde [8] based on thorough investigation of species records, information about regional distribution using previous publications, herbarium collections, and field observations by our group between 2016 and 2019. As a result, bryophyte composition, endemism, growth forms, and diversity comparisons among different islands are also reported. The results will contribute to improving our knowledge of bryophytes in Cape Verde, enhancing the understanding of its unique flora, and emphasizing the imperative need for conservation efforts.

2. Materials and Methods

2.1. Literature Review

This paper is based on published data on the current Cape Verde list [8], along with significant contributions from Frahm et al. [11], González-Mancebo et al. [12], Ellis et al. [13,14], Cano [15], Jiménez and Cano [16], Sérgio and Stow [17], Dirkse et al. [18], Sérgio and Melo [19], Sim-Sim et al. [20], and Ellis et al. [21], previously referred in Garcia et al. [9], and the more recently publication by Martins et al. [10]. The nomenclature for families and the majority of bryophyte taxa follows Hodgetts et al. [22], and Wigginton [23], for African liverwort and hornwort taxa (Classes Anthocerotopsida, Jungermanniopsida, and Marchantiopsida) and O’Shea [6] for the mosses (Class Bryopsida), with exceptions including Cano [15], for Tortula solmsii, Jiménez and Cano [16] for Didymodon caboverdensis, Luna [24], for Hedwigidium integrifolium, and Martins et al. [10] for Exormotheca martins-loussaoae Sim-Sim, A.Martins, J.Patiño & C.A.Garcia.

2.2. Field Sampling and Herbarium Material

Bryophyte sampling took place in the Cape Verde archipelago between 2016 and 2019 (Figure 1), with a total of 56 sites sampled on the islands of Santo Antão (31 sites), São Vicente (6 sites), and São Nicolau (19 sites). More sites were studied on Santo Antão due to its higher diversity of habitats favorable to the growth of bryophytes. In these three islands, a range of habitats was investigated, including soil, rocks, epiphytes, and aquatic communities [9]. Additionally, the selection of areas for fieldwork in Cape Verde was based on information provided by herbarium materials, as well as the fieldwork experience of bryologists from the MUHNAC (Museu Nacional de História Natural e da Ciência da Universidade de Lisboa) in the Macaronesian region [2,25]. Most of the fieldwork was conducted in the National Parks (e.g., Parque Natural de Cova-Ribeira da Torre-Paul, Santo Antão; Monte Gordo, São Nicolau; Monte Verde, São Vicente), above 500 m a.s.l. These areas host extensive bryophyte communities, consistent with the presence of rich vegetation [26]. In contrast, bryophyte communities are scarce in lower areas due to long periods of severe drought. Thus, our sampling sites (42 out of 56) were randomly located at elevations ranging from 500 m a.s.l. to 1580 m, using 0.5 m × 0.5 m plots. Within each 0.5 m × 0.5 m plot, representative samples of all bryophytes were collected, and information about elevation, geographic coordinates, substrate, and habitat were recorded in the field. The collected specimens are stored at the Herbarium LISU Herbarium (University of Lisbon, MUHNAC).

2.3. Data Analysis

In the present study, for each taxon referred to Cape Verde or collected by us, its distribution in the archipelago, endemicity, and growth forms are presented in Appendix A. The distribution per island follows the order from north to south and from west to east: Santo Antão, São Vicente, Santa Luzia, São Nicolau, Sal, Boavista, Maio, Santiago, Fogo, and Brava. For some species, the islands are not indicated due to a lack of information about their distribution. Some taxa are annotated with numbers corresponding to notes, which are linked to certain aspects, such as taxonomy, nomenclature, distribution, or new taxa records after Patiño and González-Mancebo [8]. Additionally, a list of the primary synonyms for the bryoflora of Cabo Verde is provided. Furthermore, three taxa are excluded from the archipelago, and two are considered doubtful (Appendix A).

Bryophytes were categorized into the two major lineages of bryophytes: liverworts and mosses. Since the number of hornworts was limited to two species, this lineage was combined with liverworts for the subsequent analyses. Furthermore, liverworts and mosses were classified based on two different growth forms: leafy or thalloid liverworts and acrocarpous or pleurocarpous mosses, respectively. These four groups exhibit distinct tolerances to drought. Leafy liverworts and pleurocarpous mosses are globally better adapted to shaded and humid environments [27]. In contrast, thalloid liverworts and acrocarpous mosses typically exhibit broader ecological requirements, thriving in sunnier, drier, and more xeric habitats [27,28].

We employed a chi-square test to assess whether the observed distributions of bryophyte growth form groups (in Cape Verde and per island) significantly deviated from a uniform distribution. This analysis was performed using the “stats” R package version 4.5.0. [29].

3. Results

3.1. Updated List

This new list provides a comprehensive inventory of the bryophytes found in the Cape Verde archipelago, offering an overview of the acceptance of species and infraspecific names. We present a list of accepted names and report synonyms used in the bibliography to guide readers toward accepted names in this updated list (Appendix A).

There are 185 accepted bryophyte taxa in this list, comprising 175 species, 5 subspecies, and 5 varieties, totaling 49 liverworts (including 2 hornworts) and 136 mosses. This corresponds to 93 bryophyte genera (25 liverwort genera, including hornworts, and 68 moss genera) and 42 families (18 liverwort families, including hornworts, and 24 moss families) (Appendix A).

Three species are excluded from the flora of Cape Verde: Exormotheca pustulosa Mitt., Ptychomitrium subcrispatum Thér. & P. de la Varde, and Barbula javanica Dozy & Molk. (Appendix A).

In this study, 34 new taxa are added to the Cape Verde bryophyte list, namely 13 liverworts (Aneura pinguis (L.) Dumort.; Cheilolejeunea rigidula (Nees ex Mont.) R.M.Schust.; Cheilolejeunea xanthocarpa (Lehm. & Lindenb.) Malombe; Exormotheca martins-loussaoae Sim-Sim, A.Martins, J.Patiño & C.A.Garcia; Pleurozia gigantea (F.Weber) Lindb.; Porella canariensis (F.Weber) Underw.; Riccia atromarginata Levier; Riccia atropurpurea Sim; Riccia congoana Stephani; Riccia crinita Taylor; Riccia macrocarpa Levier; Riccia trabutiana Steph.; Syzygiella manca (Mont.) Steph), and 21 mosses (Aloina ambigua (Bruch & Schimp.) Limpr.; Bartramia aprica Müll. Hal. Brid.; Bryoceuthospora aethiopica (Welw. & Duby) R.H.Zander; Bryum dichotomum Hedw.; Crossidium geheebii (Broth.) Broth.; Cryphaea heteromalla (Hedw.) D.Mohr; Didymodon caboverdeanus J.A.Jiménez & M.J.Cano; Didymodon revolutus (Cardot) R.S.Williams; Didymodon tophaceus subsp. sicculus (M.J.Cano, Ros, García Zam. & J.Guerra) Jan Kučera; Entosthodon kroonkurk Dirkse & Brugués; Grimmia incurva Schwägr.; Homalothecium aureum (Spruce) H.Rob.; Lewinskya acuminata (H.Philib.) F.Lara, Garilleti & Goffinet; Lindbergia patentifolia Dixon; Microbryum davallianum (Sm.) R.H.Zander; Microbryum starckeanum (Hedw.) R.H.Zanderm; Timmiella cameruniae Broth.; Tortula bolanderi (Lesq. & James) M.Howe; Tortula muralis Hedw.; Tortula revolvens (Schimp.) G.Roth; Tortula vahliana (Schultz) Mont.). These new taxa are found, respectively, on the islands of Santo Antão (21), São Vicente (2), São Nicolau (2), Santiago (4), and Fogo (16) (Appendix A). In addition, one moss species (Hydrogonium arcuatum (Griff.) Wijk & Margad.) is newly recorded for Cape Verde (São Nicolau), and Africa. Some taxa previously reported for Cape Verde [8] were found on other islands of the archipelago, specifically Santo Antão (five), São Vicente (three), Santiago (nine), and Fogo (six).

3.2. Bryophyte Diversity

The largest liverworts family (i.e., taxa number > 5) is Ricciaceae (13 taxa, 1 genera) followed by Lejeuneaceae (10 taxa, 6 genera), and Frullaniaceae (5 taxa, 1 genera). Among mosses, Pottiaceae (58 taxa, 23 genera) is the largest family, followed by Bryaceae (13 taxa, 5 genera), Brachytheciaceae (10 taxa, 8 genera), Fissidentaceae (9 taxa, 1 genus), and Bartramiaceae (8 taxa, 2 genera), and Orthotrichaceae (5 taxa, 4 genera) stand out. For liverworts, Riccia leads with 13 taxa, followed by Frullania with 5 taxa. Prominent moss genera in Cape Verde include Didymodon (10 taxa), Tortula (10 taxa), Fissidens (9 taxa), Philonotis (6 taxa), and Bryum (5 taxa).

3.3. Comparing Bryophyte Diversity between Islands

Regarding the distribution of taxa by island, there are substantial differences between the Cape Verde islands in the number and proportion of taxa. The islands with the highest number of taxa are Santo Antão with 135 taxa (23 liverworts and 112 mosses), Fogo with 77 taxa (23 liverworts and 54 mosses), and São Nicolau with 76 taxa (16 liverworts and 60 mosses). Santiago totals 49 taxa (15 liverworts and 34 mosses), followed by São Vicente with 29 taxa (10 liverworts and 19 mosses) and Brava with 15 (2 liverworts and 13 mosses). No liverwort taxa are known for the islands of Sal and Boavista, with two moss taxa for Sal and one for Boavista. There are no known records of bryophytes for the islands of Santa Luzia and Maio (Figure 2). Additionally, the distribution by islands is unknown for 15 out of the 185 taxa.

3.4. Endemism

Eight bryophyte taxa are endemic to Cape Verde, including one liverwort (Exormotheca martins-loussaoae Sim-Sim, A.Martins, J.Patiño & C.A.Garcia) and seven mosses (Bryum anomodon Mont.; Didymodon caboverdeanus J.A.Jiménez & M.J.Cano; Entodon pseudoseductrix (Müll.Hal.) A.Jaeger; Fissidens allorgei P.de la Varde; Funaria chevalieri P.de la Varde; Perssonia sanguinea Bizot; Pseudoleskeopsis bollei (Broth. & Geh.) P.Rao. Santo Antão possesses the greatest abundance of endemics, with seven out of eight endemic taxa accounted for: Exormotheca martins-loussaoae, Bryum anomodon, Didymodon caboverdeanus, Entodon pseudoseductrix, Fissidens allorgei, Perssonia sanguinea, and Pseudoleskeopsis bollei. São Nicolau has five endemics: Exormotheca martins-loussaoae, Entodon pseudoseductrix, Fissidens allorgei, Perssonia sanguinea, and Pseudoleskeopsis bollei. Fogo also has five endemics: Exormotheca martins-loussaoae, Bryum anomodon, Didymodon caboverdeanus, Entodon pseudoseductrix, and Funaria chevalieri. Santiago has three endemic species: Bryum anomodon, Didymodon caboverdeanus, and Perssonia sanguinea. São Vicente and Sal islands each have one endemic taxa: Pseudoleskeopsis bollei and Fissidens allorgei, respectively.

3.5. Bryophyte Growth Forms

In Cape Verde, acrocarpous mosses (108 taxa, 58.4%) constitute the most common bryophyte growth form (Figure 3), followed by pleurocarpous mosses, thalloid liverworts (28 taxa, 15.1% each) and leafy liverworts (21 taxa, 11.4%). The observed distributions of bryophyte growth form groups in Cape Verde are not uniformly distributed and significantly differed from the uniform distribution (χ² = 110.63, p-value < 0.0001). The proportion of acrocarpous mosses for each island, in descending order, is as follows: Brava (11 taxa, 73.3%), Santo Antão (90 taxa, 66.7%), Fogo (51 taxa, 66.2%), São Nicolau (49 taxa, 64.5%), Santiago (30 taxa, 61.2%), and São Vicente (13 taxa, 44.8%). The only moss taxa present in Sal (two taxa) and Boavista (one taxon) are acrocarpous mosses. Pleurocarpous mosses are more prevalent on São Vicente (6 taxa, 20.7%), followed by Santo Antão (22 taxa, 16.3%), São Nicolau (11 taxa, 14.5%), Brava (2 taxa, 13.3%), Santiago (4 taxa, 8.2%), and Fogo (3 taxa, 3.9%). Regarding liverworts, thalloid liverworts are more abundant on Fogo (16 taxa, 20.8%), followed by Santo Antão (17 taxa, 12.6%), Santiago (6 taxa, 12.2%), São Nicolau (9 taxa, 11.8%), Brava (1 taxon, 6.7%), and São Vicente (1 taxon, 3.4%). Leafy liverworts are more prevalent on São Vicente (nine taxa, 31.0%), followed by Santiago (nine taxa, 18.4%), São Nicolau (seven taxa, 9.2%), Fogo (seven taxa, 9.1%), Brava (one taxon, 6.7%), and Santo Antão (six taxa, 4.4%). The distributions of bryophyte growth forms per island are not uniform and show significant deviation from a uniform distribution (10.59 ≤ χ² ≤ 128.97, p-value < 0.014). Notably, São Vicente stands out as the island where the distribution most closely aligns with a uniform pattern (χ² = 10.59, p-value = 0.014).

4. Discussion

This list results from an extensive survey of the literature, incorporating personal taxonomic expertise. It represents the current understanding of taxa and recent information on species records. The total number of accepted bryophyte taxa in Cape Verde adds to 185, consisting of 175 species, 5 subspecies, and 5 varieties, encompassing 49 liverworts (including 2 hornworts) and 136 mosses. Santo Antão, São Nicolau, and Fogo exhibit high bryophyte diversity, with the largest number of genera and families found on these islands. The moss families with the highest number of genera are Pottiaceae, Brachytheciaceae, and Bryaceae, with 23, 8, and 5 genera, respectively. In liverworts, Lejeuneaceae, with six genera, is the most prominent, followed by Aytoniaceae with four genera.

Santo Antão has the highest number of endemic species (seven out of eight endemic species), followed by São Nicolau and Fogo, each with five endemics. Santiago has three endemics, while São Vicente and Sal islands each have one. Endemic occurrences in the remaining islands (Boavista, Brava, Maio, and Santa Luzia) are unknown.

In Cape Verde, acrocarpous mosses constitute the most common bryophyte growth form (58.4%), followed by pleurocarpous mosses, thalloid liverworts (15.1% each), and leafy liverworts (11.4%). This distribution of bryophytes by growth form differs compared to the northern Macaronesian archipelagos, particularly in the growth forms of liverworts. In northern Macaronesia, leafy liverworts represent about 22% of the total bryoflora, while thalloid liverworts are only 9% [30,31]. It is also important to highlight the absence of leafy liverworts in Cape Verde from families well represented in the northern Macaronesian archipelagos, such as Calypogeiaceae, Jungermanniaceae, Plagiochilaceae, and Scapaniaceae [2,30,31,32,33]. The higher percentage of leafy liverworts in northern Macaronesia, which are adapted to shaded and humid environments [27], is attributed to the extensive laurel forest area, particularly on Madeira Island [2]. This unique forest is characterized by high levels of relative humidity (75–90%) nearly all year round [1,2]. The cloud layer resulting from the cooling of northeast trade winds is of vital importance for the maintenance of the bryophyte high diversity in the laurel forest [1].

In Cape Verde, São Vicente stands out as the island most similar to northern Macaronesia in terms of bryophyte composition based on growth forms. In fact, acrocarpous mosses are the predominant growth form, followed by leafy liverworts, pleurocarpous mosses, and thalloid liverworts, a pattern consistent with northern Macaronesian archipelagos [30,31]. Despite the generally low rainfall on São Vicente compared to other islands in the Barlavento group [34], the orography of this island favors the direct exposure to the prevailing trade winds. This influence is particularly evident in the Monte Verde area, where the largest bryophyte communities are found. The sloping surface of Monte Verde, facing northeast, creates an environment favorable to the incidence of humidity [34], explaining the higher percentage of leafy liverworts on São Vicente.

This study is an important contribution to our understanding of bryophyte biodiversity in Macaronesia, enhancing knowledge of biogeographic connections and the origin of the bryophyte flora in southern Macaronesia. Bryophytes are spore-producing plants with high vagility and dispersal capabilities, coupled with a remarkable variety of mechanisms of vegetative reproduction. Contrary to the classical explanation of (disjunct) distribution ranges of bryophytes by ancient vicariance (continental drift), these are nowadays assumed to be mainly shaped by long-distance dispersal events [35]. This is reflected, for example, in the postglacial history of several Macaronesian bryophyte populations, with a complex mixture of origins [7,35] and recent divergence times being incongruent with vicariance scenarios.

Unlike the northern Macaronesian archipelagos, Cape Verde’s bryophyte flora includes 20% of tropical elements. Molecular studies on Cape Verde are emerging [36], but the lack of knowledge regarding phylogenomics, biogeographic affinities, and colonization patterns hinders inferences about the origin and evolutionary history of the southern Macaronesian flora. This knowledge is crucial for understanding the effects of climatic changes on future plant colonization in this region. The morphological and molecular analyses of the liverwort genus Exormotheca [36], indicate a complex evolutionary pattern, including an Africa–Cape Verde connection and a Rand Flora pattern [37]. Exormotheca probably originated in south-east Africa during the Oligocene. Climate-driven vicariance (due to aridification and orogenic movements in Africa) and long-distance dispersal events appear to have driven the current disjunction. While the northern Macaronesian archipelagos share the same lineage, Cape Verde was colonized by a distinct lineage. Consequently, the hypothesis that Cape Verde may have acted as a crossroads, linking northern Macaronesia and south-east Africa, is not supported. These results clearly indicate the need to trace past colonization events of Cape Verde bryophyte taxa.

Our work reflects the state of knowledge as of February 2024 and is likely to be updated. Progress in phylogenetics may alter the status of known taxa, and new species continue to be discovered. To preserve Cape Verde’s biodiversity, efficient implementation of laws and regulations is essential, along with increased support in terms of human resources and financial endowment.