Botanica Marina 2017; 60(5): 583–589

Short communication

José Martínez-Garrido*, Joel C. Creed, Samir Martins, Carmen H. Almada and Ester A. Serrão

First record of Ruppia maritima in West Africa supported by morphological description and phylogenetic classificationDOI 10.1515/bot-2016-0128Received 5 December, 2016; accepted 30 June, 2017; online first 28 July, 2017

Abstract: Ruppia maritima (widgeon grass) has been identified phylogenetically for the first time from West Africa (Santiago Island, Cape Verde). Genetic markers distinguished this species from the tetraploid Ruppia cf. maritima previously known from West Africa. Taxonomic description, photographs and molecular phylogenetic classification are provided here. The results show that, in Cape Verde, the species is phylogenetically closer to European and northeast American than to Indo-Pacific populations. This study extends the known distribution of R. maritima, an ecosystem structuring species that pro-vides essential habitat for threatened animals.

Keywords: molecular phylogenetic; morphological traits; Ruppia genus; seagrass; waterbirds.

The Cape Verde archipelago is situated off the West Africa coast in the southernmost part of the Macaronesian region. In contrast to other tropical and subtropical coastlines

where seagrass species are frequent, only a single seagrass species, Halodule wrightii Ascherson, has been recorded recently in the archipelago (Creed et al. 2016).

Ruppia (Ruppiaceae) is the only genus included in the “World Atlas of Seagrasses” (Green and Short 2003), for which distribution range maps were not presented because of the lack of existing data. It occurs in shallow habitats such as coastal lagoons, wetlands and salt-marshes (Verhoeven 1979). Meadows formed by Ruppia play a key ecological role in the trophic network of aquatic ecosystems. They also provide shelter and food for inver-tebrates, fishes, aquatic birds, marine mammals and rep-tiles such as the threatened green turtle Chelonia mydas Linnaeus (Kantrud 1991, Hemminga and Duarte 2000, Lopez-Calderon et al. 2010).

Phylogenetic and morphological studies have pro-vided new insights into the complex evolutionary history of the genus Ruppia with polyploidization, hybridization and introgression events (Ito et al. 2010, 2013, Triest and Sierens 2014, Martínez-Garrido et  al. 2016). These evo-lutionary phenomena have resulted in different criteria being used to determine which clades are considered line-ages or species. Ito et al. (2013) considered the cosmopoli-tan Ruppia maritima complex to contain lineages rather than species. However, some of these species had previ-ously been well supported by morphological and ecologi-cal studies (Verhoeven 1979, Talavera and García-Murillo 2010), for example, Ruppia drepanensis Tineo ex Guss (i.e. the “Drepanensis” clade of Ito et al. 2013) and R. maritima (i.e. the “Diploid” clade of Ito et  al. 2013). In contrast to Ito et al. (2013), other authors consider the diploid R. mar-itima (i.e. “Diploid” clade of Ito et al. 2013) to be a species distinct from several others in this complex, clearly sup-ported by both nuclear (internal transcribed spacer) and chloroplast (psbA-trnH) markers (Triest and Sierens 2014, Martínez-Garrido et al. 2016). Hybridization processes are one of the causes of this controversy. Although R. maritima presents a distinctive and unique chloroplast haplotype, its nuclear haplotype is present in other species that are putative hybrids, such as Ruppia cf. maritima. Although

*Corresponding author: José Martínez-Garrido, Biogeographical Ecology and Evolution, Centro de Ciências do Mar (CCMAR), Universidade do Algarve, Gambelas, 8005-139 Faro, Portugal; and Departamento de Ciencias del Mar y Biología Aplicada, Universidad de Alicante (DCMBA, UA), P.O. Box 99, 03080 Alicante, Spain, e-mail: jmgarrido99@gmail.com. http://orcid.org/0000-0001-9736-7930Joel C. Creed: Laboratório de Ecologia Marinha Bêntica, Departamento de Ecologia, IBRAG, Universidade do Estado do Rio de Janeiro, Rua São Francisco Xavier, 524, PHLC, Sala 220, CEP. 20550-900, Maracanã, Rio de Janeiro, RJ, BrazilSamir Martins: BIOS.CV, Sal-Rei, P.O. 52111, Boa Vista Island, Republic of Cape VerdeCarmen H. Almada: Faculdade de Ciências e Tecnologia, Departamento de Ciência e Tecnologia, Universidade de Cabo Verde, Campus do Palmarejo, C.P. 279, Praia, Republic of Cape VerdeEster A. Serrão: Biogeographical Ecology and Evolution, Centro de Ciências do Mar (CCMAR), Universidade do Algarve, Gambelas, 8005-139 Faro, Portugal

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morphologically similar to diploid R. maritima, R. cf. mar-itima differs in the chloroplast haplotype and chromosome number (Ito et al. 2013, Triest and Sierens 2014, Martínez-Garrido et  al. 2016). Despite the different taxonomic approaches to the clades, all these studies have shown a great diversity in the Ruppia genus and clearly distinct genetic entities, some of which have a hybrid origin.

According to the bioregional model of seagrass dis-tribution of Short et  al. (2007), R. maritima Linnaeus is expected to occur in all biogeographical regions. However, the difficulty in properly identifying species and the traditional use of R. maritima as a catch-all taxon may have resulted in an exaggerated distributional range of R. maritima and a underestimation of Ruppia species diversity (den Hartog and Kuo 2006, Triest and Sierens 2014). The type of R. maritima was collected by Linnaeus in the Baltic Sea and corresponds to the “Diploid” clade of Ito et  al. (2013) and to the R. maritima of Triest and Sierens (2014) and of Martínez-Garrido et  al. (2016). The distribution range of this R. maritima, sensu stricto needs to be accurately determined based on morpho-logical and phylogenetic analyses (Short et  al. 2010,

Triest and Sierens 2015). This will enable the biogeo-graphical ranges and putative hybridization zones with other Ruppia species to be described, thereby helping to define species distributions and evolutionary history better.

In 2015, R. maritima was found at Lagoinha, Santiago Island, Cape Verde (15°7′40.66″ N, 23°31′15.15″ W) growing in one of two lagoons of the Pedra Badejo wetland (Ramsar Site n° 1577; Figure 1). These lagoons are fed mainly by seawater that reaches them during high tides. They are an important habitat for migratory birds, and the adjacent beach is one of the most important nesting beaches for the endangered loggerhead seaturtle (Caretta caretta Lin-naeus) on the island (Veiga et al. 2015).

To obtain photographs and morphological data, 10  specimens were haphazardly sampled along a 100-m linear transect. The morphological description is based on minimum, mean and maximum measures of specimens, based on four replicate measurements per specimen of a suite of taxonomic characters as defined according to descriptions in Oliveira et  al. (1983), Kantrud (1991) and Flora Ibérica (Talavera and García-Murillo 2010). The total

Figure 1: Map of the Cape Verde Islands, and detail of the Ruppia maritima site at Santiago Island (black square).

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number of measurements for each taxonomic character were as follows: 40 for internode length, leaf length, leaf width and leaf sheath length; 39 for rhizome diameter and root length; 36 for inflorescence peduncle length, fruitlet length, podogyne length and number of mature fruitlets per inflorescence; 35 for fruitlet width; 34 for fruitlet beak

length; 33 for peduncle diameter; 10 for plant height; 9 for number of fruitlets per plant; 8 for carpel length; and 2 for anther length.

A morphological description of the sampled popu-lation is provided here: submerged herbaceous plant (Figure 2A–C). Plants 27–109  cm in height: Rhizome

A C

D E

GF

H I

B

Figure 2: Ruppia maritima: photographs of specimens from Santiago Island.(A) Sampled population of R. maritima; (B) detail of the biomass accumulation; (C) R. maritima with flowers and fruits; (D) acute leaf tip; (E) leaf cross-section showing the central nerve; (F) inflorescence showing anthers and gynoecium; (G) detail of the four carpels of each flower; (H) detail of a mature fruitlet; (I) infructescence showing elongated podogynes and six mature fruitlets. Photographs are by the authors, except (C) by Peter Wirtz, used with permission.

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Figure 3: Ruppia maritima samples from Santiago Island.Phylogenetic classification of the specimens when compared to the samples used in Martínez-Garrido et al. (2016). (A) Phylogenetic cor-respondence based on chloroplast psbA-trnH. (B) Phylogenetic correspondence based on nuclear internal transcribed spacer (ITS) regions. All accessions show the sample’s origins, the species names used by the authors and, in parentheses, the authors that deposited the sequences (I, Ito et al.; T, Triest and Sierens; MG, Martínez-Garrido et al.). New accessions deposited in the present study are shown in bold type and emphasized in large font, with the species names identified by morphology according to the taxonomic criteria of the Flora Ibérica (Talavera and García-Murillo 2010) and descriptions in Oliveira et al. (1983) and Kantrud (1991). Bootstrap support is indicated as numbers at the branches. The names listed between psbA-trnH and ITS trees are the taxonomic conclusions proposed by Martínez-Garrido et al. (2016), Ito et al. (2013) and Triest and Sierens (2014). The two groups supported by ITS and psbA-trnH markers in the R. maritima clade are boxed and marked with vertical labels (IPG, Indo Pacific Group; ENAG, European and Northeast America Group). Accession numbers of sequences 0–32 are listed in Martínez-Garrido et al. (2016). Samples labeled #1 and #2 show heterogeneous ITS sequences. New acces-sion numbers from the present study (No. 33) are KY002069-KY002070. DNA extraction, molecular markers amplification and phylogenetic analyses were conducted as described in Martínez-Garrido et al. (2016).

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(0.6–) 0.7 (−0.9) mm in diameter; internodes (1.8–) 3.9 (−10.8) cm long; root (0.8–) 6.1 (−17) mm in length. Leaves linear (6–) 10.3 (−21.1) mm in length and (0.2–) 0.4 (−0.6) mm wide with acute tips (Figure 2D), and a single nerve (Figure  2E), leaf sheath not transpar-ent (0.6–) 1.2 (−2.0) cm long. Peduncle supporting the inflorescence not coiled, with diameter (0.3–) 0.4 (−0.6) mm and length (10–) 19.4 (−46) mm at anthesis. Inflo-rescence with two hermaphrodite flowers, each with an apocarpic gynoecium, anthers 0.6–0.7 mm long (Figure 2F), four carpels per flower (0.5–) 0.7 (−1.0) mm long (Figure 2G), stigma wider than the ovary before fruit-ing. Fruitlet drupaceous, (1.5–) 2.0 (−2.5) cm in length and (1–) 1.4 (−1.8) cm wide (Figure 2H); fruitlet beak (0.2–) 0.4 (−0.6) mm in length, podogynes (5–) 10 (−20) mm long (Figure 2I). Each inflorescence had from two to eight mature fruitlets (Figure 2I), and each plant had (19–) 75.4 (−180) fruitlets. A reference herbarium speci-men (14809/ALGU) was deposited at the University of Algarve, Portugal.

For the phylogenetic classification, the sequenced psbA-trnH (chloroplast) region was 305 base pairs (bp) long, and the Internal Transcribed Spacer (ITS) (nuclear) region was 652 bp in length. Both psbA-trnH (Figure 3A) and ITS (Figure 3B) sequences obtained from the Cape Verde samples showed congruent results and correspond to the species R. maritima (Figure 3). The R. maritima clade is composed of two groups supported by both ITS and psbA-trnH sequenced regions (except for the East South Africa sample), and the Cape Verde samples were associ-ated with the European (France and Finland) and north-east America (Maryland, USA, and Nova Scotia, Canada) group rather than with that from the Indo-Pacific (China, India, Vanuatu; Figure 3).

Phylogenetic analyses are necessary because the des-ignation R. maritima has been used for distinct species in the past (Triest and Sierens 2014, Martínez-Garrido et al. 2016). This study adds to the little that is known of Ruppia on the African continent and provides the first record of R. maritima in West Africa confirmed by morphology and phylogenetic delimitation. Previously, R. maritima had been determined only from the East coast of South Africa (Natal, St Lucia Bay; Triest and Sierens 2014; included in Figure 3). What was previously identified as R. maritima from Morocco (North West Africa; sample not shown in Figure 3) corresponds genetically to another species, which was designated in that study as “Tetraploid” (Ito et al. 2010); R. maritima from South Africa described by Cook (2004) was also genetically identified as “Tetraploid α” (Ito et  al. 2015), and this is the species we designate as Ruppia cf. maritima (Martínez-Garrido et al. 2016; see

Figure 3). Ruppia maritima has also been listed for the Azores (Morton et  al. 1995), the Canaries (Santos and Fernández 1984), Cape Verde (Sánchez-Pinto et al. 2005), the Oranjemund wetland in Namibia ( Williamson 1997), the Keta coastal lagoon in Ghana (Lamptey and Armah 2008) and at different sites in South Africa (Cook 2004, see Ito et al. 2015). However, these studies did not present supporting morphological descriptions and phyloge-netic analyses, and therefore a precise species cannot be assigned.

The complete taxonomic description included in this study can be used as a guide to help researchers identify R. maritima based on morphological traits. Additionally, the genetic analyses have allowed us to circumscribe the Cape Verde samples in the phylogenetic clade of R. maritima, discriminating this species from the morpho-logically similar Ruppia cf. maritima detected in other African, Mediterranean and Iberian locations (“Tetra-ploid α” of Ito et al. 2013; “haplogroup E” of Triest and Sierens 2014, Ruppia cf. maritima of Martínez-Garrido et  al. 2016). Although both species present similar nuclear ITS haplotypes, their organelles (studied using chloroplast DNA markers) are phylogenetically distant. This is due to past hybridization in the likely allopoly-ploid speciation origin of tetraploid R. cf. maritima (Triest and Sierens 2014, Martínez-Garrido et al. 2016 referred as “haplogroup E”).

The source of R. maritima in Cape Verde is unknown, and it has been previously described as a “probable native” in Sal and Boa Vista Islands (Sánchez-Pinto et al. 2005). However, as R. maritima likely did not evolve on the volcanic islands of Cape Verde, it probably colonized them from unknown nearby populations in West Africa, with similar haplotypes to the European and northeast American populations. Species of Ruppia are known to be dispersed by seabirds and ocean currents (Figuerola et al. 2002, Triest and Sierens 2013). As the main ocean currents on the West African coast near Cape Verde run from north to south, it seems probable that aquatic birds could be the main dispersal vector. The location where R. maritima was sampled is visited by a great number of waterbirds, the main migratory bird group in the archipelago (Veiga et  al. 2015). Previous studies in South Africa and the Iberian Peninsula have detected Ruppia seeds in the diet of several ducks and coots, and these seeds maintained their capacity to germinate after being defecated (Figuerola et  al. 2002, Reynolds and Cumming 2016). Studies using microsatellites in R. mar-itima (Triest and Sierens 2015) and in Ruppia cirrhosa (Petagna) Grande (Martínez-Garrido et  al. 2017) have also proposed waterbirds as the dispersal vector, so this

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hypothesis should be further investigated with more genetic markers and samples from more locations.

Acknowledgments: We thank Cymon Cox for manuscript revision and Peter Wirtz for helping with the collection and for providing the photo. This study was made pos-sible given the support from the Instituto Gulbenkian de Ciência (program PGCD), Portugal, and the Cape Verde University. It was also funded by FCT, the Portuguese Sci-ence Foundation (CCMAR-UID/Multi/04326/2013) and the Pew Foundation Marine Fellow program (EAS). JCC was supported by CAPES (Ciências do Mar 1137/2010), FAPERJ (E26/201.286/2014), and CNPq (305330/2010-1).

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BionotesJosé Martínez-GarridoBiogeographical Ecology and Evolution, Centro de Ciências do Mar (CCMAR), Universidade do Algarve, Gambelas, 8005-139 Faro, Portugal; and Departamento de Ciencias del Mar y Biología Aplicada, Universidad de Alicante (DCMBA, UA), P.O. Box 99, 03080 Alicante, Spain, http://orcid.org/0000-0001-9736-7930.jmgarrido99@gmail.com

José Martínez-Garrido is a PhD student at the Department of Marine Science and Applied Biology in Alicante University (Spain) and the Biogeographical Evolution and Ecology group of Centro de Ciências do Mar in Portugal. His PhD study is focused on the systematics, speciation processes and genetic structure of the genus Ruppia. Over the last years, he has participated in molecular ecology and biodiversity projects of marine plants, algae and animals. He is also interested in the implications of this knowledge in the effective management of marine biodiversity.

Joel C. CreedLaboratório de Ecologia Marinha Bêntica, Departamento de Ecologia, IBRAG, Universidade do Estado do Rio de Janeiro, Rua São Francisco Xavier, 524, PHLC, Sala 220, CEP. 20550-900, Maracanã, Rio de Janeiro, RJ, Brazil

Joel C. Creed is an associate professor at the State University of Rio de Janeiro. Dr. Creed graduated in Botany with Marine Botany (Uni-versity of Wales Bangor, UK) in 1989 and received his PhD in 1993 at the University of Liverpool, UK. His research focuses on the biology and ecology of marine plants and invertebrates on rocky shores and coral reefs, and in seagrass and macroalgae habitats. He has been coauthor on 69 publications in these fields.

Samir MartinsBIOS.CV, Sal-Rei, P.O. 52111, Boa Vista Island, Republic of Cape Verde

Samir Martins is a conservation biologist from Cabo Verde Islands, with a special interest in animal ecology. His research interest is focused on sea turtle response to environmental changes and the

effects on offspring survival. He has participated actively in all aspects and phases of important projects regarding Cape Verde sea turtle conservation. Currently, he is involved in conservation activi-ties for all endangered species (sea turtles, whales and birds) and a Marine Protection Area, the definition of ecotourism guidelines and information, education and awareness activities addressed to the local people in as well as visitors of Boa Vista Island, Cabo Verde.

Carmen H. AlmadaFaculdade de Ciências e Tecnologia, Departamento de Ciência e Tecnologia, Universidade de Cabo Verde, Campus do Palmarejo, C.P. 279, Praia, Republic of Cape Verde

Carmen H. Almada has a PhD in Coastal Zone Management, an MSc in Ecology and a BA in Marine Biology. Her PhD thesis deals with the flora and ecology of the benthic algae of the Cape Verde Islands. She is a biologist specializing in marine botany, with experience in phycology. She has also conducted research at University of Gran Canaria (Spain) and Federal University of Rio de Janeiro (Brazil). At present, her research is centered on the study of macroalgae and seagrasses of the Cape Verde Islands, with a focus on taxonomy, ecology and conservation.

Ester A. SerrãoBiogeographical Ecology and Evolution, Centro de Ciências do Mar (CCMAR), Universidade do Algarve, Gambelas, 8005-139 Faro, Portugal

Ester A. Serrão (lecturer at the University of Algarve) coordinates a research team at CCMAR-Centre for Marine Sciences, which aims to understand patterns and processes mediating marine genetic diversity, function and evolution, from ecological to deep evolution-ary scales. Her research topics include causes and consequences of genetic biodiversity, population dispersal/connectivity, environ-mental genomics and adaptive evolution, in the context of climate and environmental change. These are studied across the diversity of marine systems ranging from microorganisms to large marine forests.

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