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Hidrobiológica

versão impressa ISSN 0188-8897

Hidrobiológica vol.27 no.3 México Set./Dez. 2017

 

Articles

Species diversity and biogeographical patterns of Laurencia sensu stricto (Rhodophyta) in the Atlantic Ocean

Diversidad de especies y patrones biogeográficos de Laurencia sensu stricto (Rhodophyta) en el océano Atlántico

Oscar E. Hernández1  2  * 

Abel Sentíes2 

Kurt M. Dreckmann2 

Valéria Cassano3 

Mutue T. Fujii4 

1 Estudiante del Doctorado en Ciencias Biológicas y de la Salud. Universidad Autónoma Metropolitana, Unidad Iztapalapa. A.P. 55-535, CDMX, 09340, Mexico

2 Departamento de Hidrobiología, Universidad Autónoma Metropolitana, Unidad Iztapalapa. A.P. 55-535, CDMX, 09340, Mexico

3 Departamento de Botânica, Universidade de São Paulo, Rua do Matão 277, São Paulo 05508-090, Brazil

4 Núcleo de Pesquisa em Ficologia, Instituto de Botânica, Av. Miguel Estéfano, 3687-04301-902 São Paulo, Brazil

Abstract

Background:

Recent morphological and phylogenetic studies of Laurencia in the Atlantic Ocean have modified our cu rrent knowledge of the group. Approximately 23% of the worldwide generic diversity has been recorded in this region.

Goals:

Update the checklist of the Laurencia species in the Atlantic and describe the distribution patterns within the ge nus.

Methods:

We obtained records of Laurencia species in the Atlantic from a review of the literature and distributional data were used to define areas of endemism through a PAE (Parsimony of Areas of Endemism) analysis.

Results:

We propose an updated checklist of the 30 currently recognized species of Laurencia in the Atlantic Ocean; this checklist also includes taxonomic synonyms, nomenclatural remarks, and a detailed distribution for each species. The distributional range for the genus in the Atlantic extends from Bermuda and Northern Europe in the North Atlantic to Brazil and South Africa in the South Atlantic. We were able to define four areas of endemism: Brazil with four endemic species, the Gulf of Guinea with four endemic species, the northeastern Atlantic with three endemic species, and South Africa with four endemic species; also documented was one secondary area (Macaronesian Islands) with the endemic species L. viridis. Moreover, 17 of the 30 species of the Atlantic are also distributed in the Indo-Pacific, of which five are amphi-Atlantic species.

Conclusions:

The patterns found are related to geological events that occurred in the past, a fact that allows us to formulate a vicariance hypothesis about these species biogeographic history. Therefore, future work that will document new species and the clarification of taxonomic problems will allow researchers to continue enriching this hypothesis.

Key words: Area of endemism; biogeography; PAE analysis; red algae

Resumen

Antecedentes:

Los recientes estudios morfológicos y filogenéticos de Laurencia para el océano Atlántico han modificado el conocimiento actual sobre la diversidad del grupo, registrándose para esta región, aproximadamente el 23% de la diversidad del género a nivel mundial.

Objetivos:

Actualizar el listado de especies de Laurencia presentes en el Océano Atlántico y definir sus patrones de distribución.

Métodos:

Se obtuvieron los registros de las especies del género a partir de una revisión bibliográfica, utilizando los datos de distribución para la definición de patrones biogeográficos mediante un análisis de PAE.

Resultados:

Se propone un listado actualizado que contiene 30 especies de Laurencia reconocidas taxonómicamente para el Océano Atlántico; además se incluyen sinónimos, notas nomenclaturales y la distribución a de talle de cada una de las especies. El intervalo de distribución del género se extiende desde Bermuda y el norte de Europa para el Atlántico Norte, hasta Brasil y Sudáfrica en el Atlántico Sur. Se definieron cuatro áreas de endemismo: Brasil con cuatro especies endémicas, Golfo de Guinea con cuatro especies restringidas, Noreste del Atlántico con tres especies endémicas y Sudáfrica con cuatro especies endémicas; además de un área secundaria (Islas de la Macaronesia) con L. viridis como especie endémica. Por otro lado, 17 de las 30 especies registradas para el Atlántico se distribuyen también en el Indo-Pacífico, de las cuales cinco son especies anfi-Atlánticas.

Conclusiones:

Los patrones encontrados han sido relacionados con eventos geológicos que han ocurrido en el pasado, permitiendo ofrecer una hipótesis de vicarianza sobre su historia biogeográfica. Por lo tanto, trabajos futuros sobre el reconocimiento de nuevas especies y el esclareci miento de problemas taxonómicos permitirá continuar enriqueciendo dicha hipótesis.

Palabras clave: Áreas de endemismo; biogeografía; Análisis de PAE; algas rojas

Introduction

There is a need for an updated checklist of Laurencia (Rhodophyta, Ceramiales) in the Atlantic Ocean that accounts for recent morphological and phylogenetic studies that have modified our current knowledge of the group. For instance, the “Laurencia complex” has replaced the former concept of Laurencia sensu lato. The genus Laurencia sensu stricto (s.s.) (Garbary & Harper, 1998; Nam, 2006; Gil-Rodríguez et al., 2012), and the following seven genera belonging to the complex (mentioned above):Osmundea Stackhouse, Chondrophycus (Tokida et Saito) Garbary et J. T. Harper, Palisada K. W. Nam, Yuzurua (K.W. Nam) Martin-Lescanne, Laurenciella Cassano, Gil-Rodríguez, Sentíes, Díaz-Larrea, M. C. Oliveira et M. T. Fujii, Coronaphycus Metti and Ohelopapa F. Rousseau, Martin-Lescanne, Payri et L. Le Gall. These genera differ in the number of pericentral cells cut off by the vegetative axial segments, the origin of spermatangial branches, and the origin of tetrasporangia from determined cells (Saito, 1967; Nam et al., 1994; Garbary & Harper, 1998; Nam, 1999, 2006, 2007). Molecular phylogenetic data also support distinction among them (Martin-Lescanne et al., 2010; Cassano et al., 2012a; Metti et al., 2015; Rousseau et al., 2017).

Laurencia comprises 130 taxonomically recognized species worldwide (Guiry & Guiry, 2017). In particular, 18 species of the genus have been recorded for the Western Atlantic (from North Carolina to Brazil) and 21 for the Eastern Atlantic (Europe and Africa). These represent 23% of the species richness worldwide. Phylogenetic studies of some Laurencia species in the Atlantic have shown the artificiality of the wide ranges of distribution of some species, such as L. microcladia and L. obtusa (Cassano et al., 2012a) that have been eliminated from the Bra zilian flora.

The area of endemism is defined as the sympatric congruence between two or more endemic species, based on the fact that the se species share a common spatial history (Platnick, 1991; Morrone, 2007). Other areas that can be documented are the secondary areas, which have only one endemic species or the so-called relic species that are important because these areas may be later isolations where spe cies radiation has not yet occurred (Ippi & Flores, 2001; Vargas et al., 2008). The PAE (Parsimony Areas of Endemism) analysis is a method that allows us to identify areas of endemism from area cladograms. In a manner similar to phylogenetic systematics, at least two synapo morphic characters (restricted species) will define areas of endemism (Morrone, 2013).

One important outcome of this taxonomic updating is to provide a better understanding of the biogeographical patterns. With the present updated checklist, we will discuss endemism and the widespread geo graphic distribution of Laurencia species in the Atlantic.

Materials and methods

Records for Laurencia for the Atlantic Ocean were obtained from pri mary sources (these sources are indicated for each species in Results section). We complemented information with the online database Algae Base (Guiry & Guiry, 2017). Parsimony Analysis of Endemicity (PAE; Rosen, 1988) was used in a biogeographical analysis. For this analysis, an r x c binary matrix (presence and absence) was constructed, where r (rows) displays the 17 Atlantic ecoregions proposed by Spalding et al. (2007) (Figure 1) and c (columns) contains 24 of the 30 species recorded for the Atlantic Ocean. Because they could be found practically all over the Atlantic, we did not include L. brongniartii J. Agardh, L. caducira mulosa Masuda et S. Kawaguchi, L. dendroidea J. Agardh, L. intricata J. V. Lamouroux, L. microcladia Kützing, and L. obtusa (Hudson) J.V. Lamouroux. In addition, the Macaronesian Islands were excluded from the analysis because they are considered to be a transition zone with species from other areas of Atlantic (see Haroun & Prud’homme van Reine, 1993; Tuya & Haroun, 2009), and may affect our distributional patterns (Medina, 2007). Parsimony analysis was done through a heu ristic search using TBR+TBR routines with the NONA program, using the WinClada software (Nixon, 1999). A strict consensus tree was built from the most parsimonious trees.

Figure 1 Marine ecoregions used in the PAE analysis, modified from Spalding et al., (2007): Adriatic Sea (AdS), Aghulas Bank (AghB), Bermuda (Ber), Eastern Brazil (EBr), Eastern Caribbean (Eca), Greater Antilles (GA), Gulf of Guinea Central (GGC), Gulf of Guinea Upwelling (GGU), Gulf of Guinea Western (GGW), Levantine Sea (LevS), Northeastern Brazil (NEBr), Southern Caribbean (Sca), South European Atlantic Shelf (SEAS), Southeastern Brazil (SEBr), St. Helena and Ascension Islands (SHAI), Western Caribbean (WCa), and Western Mediterranean (WMe). 

Six “species inquirenda” (L. alsidiidormis Zanardini ex Fraudenfeld, L. alsidioides P. L. Crouan et H.M. Crouan, L. botryocephala Kützing, L. canariensis Montagne ex Kützing, L. moriformis Kützing and L. trifaria Kützing) did not provide information about their geographical distri bution and were recorded only once by their respective authors. Null or limited herbarium material prevented us from being totally certain about these taxa. Categories of areas (patterns) were defined: Those containing an endemic species (Secondary Area); those with congru ence in geographical distribution of two or more endemic species (Area of Endemism), that is, clades defined by two or more synapomorphies; and widespread species (amphi-Atlantic Areas). In addition, we defined areas containing two or more endemic species without total congru ence in the geographic distribution of these, known as areas of Partial Congruence.

Results

Checklist of Laurencia species

  • Laurencia brachyclados Pilger

  • Type locality: Annobon Island, Equatorial Guinea, West Africa.

  • Distribution: Gulf of Guinea: Equatorial Guinea: Annobon Island (John et al., 2004).

  • St. Helena and Ascension Islands: Ascension Island (John et al., 2004).

  • Laurencia corymbosa J. Agardh

  • Type locality: Cape of Good Hope, South Africa.

  • Distribution: South Africa: Cape of Good Hope (Silva et al., 1996).

  • Laurencia epiphylla F. Boisset et J. C. Lino

  • Type locality: Alicante: La Granadella, Jávea, the Mediterra nean coast of Spain.

  • Distribution: Mediterranean Sea: Spain: Alicante (Gómez-Ga rreta et al., 2001).

  • Laurencia flexuosa Kützing

  • Type locality: “Ad Caput Bonae Spei”, South Africa.

  • Distribution: South Africa: Cape Town (Stegenga et al., 1997).

  • West African Transition: Mauritania [uncertain record (John et al., 2004)].

  • Laurencia foldatsii N. Rodríguez de Rios

  • Type locality: Taguao, Distrito Federal, Venezuela

  • Distribution: Tropical Northwestern Atlantic: Venezuela (Gane san, 1990).

  • Laurencia galtsoffii M. Howe

  • Type locality: Pearl and Hermes Reef, Hawaiian Archipelago.

  • Distribution: Gulf of Guinea: Gabon, Ghana, and Liberia (John et al., 2004).

  • West African Transition: Cape Verde Islands (John et al., 2004).

  • Laurencia griseaviolacea M.J. Wynne

  • Type locality: Clovelly, Cape Peninsula, South Africa.

  • Distribution: South Africa: Cape Town (Stegenga et al., 1997, as Laurencia peninsularis H. Stegenga, J. J. Bolton et R. J. Anderson not L. peninsularis Taylor).

  • Laurencia laurahuertana Mateo-Cid, Mendoza-González, Sentíes et Díaz-Larrea

  • Type locality: Punta Herrero, Quintana Roo. México

  • Distribution: Caribbean Sea and Gulf of Mexico. Mexico: Quin tana Roo (Mateo-Cid et al., 2014).

  • Laurencia minuscula Schnetter

  • Type locality: Puerto López (Alta Guajira), Guajira Department, Colombia.

  • Distribution: Tropical Northwestern Atlantic: Colombia: Guajira (Schnetter, 1976). Cuba: Havana (Sentíes et al., 2010).

  • Laurencia natalensis Kylin

  • Type locality: Isipingo Beach, near Durban, South Africa

  • Distribution: South Africa: Pearly Beach to Agulhas (Stegenga et al., 1997)

  • Laurencia nidifica J. Agardh

  • Type locality: Hawaiian Islands

  • Distribution: Gulf of Guinea: Ivory Coast,Ghana, and Liberia (John et al., 2004).

  • Lusitania: Madeira Archipelago: Deserta Grande [uncertain re cord (Neto et al., 2001)].

  • St. Helena and Ascension Islands: St. Helena (John et al., 2004).

  • West African Transition: Cape Verde Islands (John et al., 2004).

  • Laurencia oliveirana Yoneshigue

  • Type locality: Ponta da Cabeça, Cabo Frio, Rio de Janeiro State, Brazil.

  • Distribution: Tropical Southwestern Atlantic: Brazil: Rio de Janeiro (Fujii et al., 2012) and Bahia ((Fujii & Sentíes, 2005).

  • Warm Temperate Southwestern Atlantic: Brazil: Rio Grande do Sul and São Paulo (Fujii & Sentíes, 2005).

  • Laurencia tenera C. K. Tseng

  • Type locality: Shek-O, Hong Kong.

  • Distribution: Gulf of Guinea: Ivory coast, Ghana, Liberia, Sierra Leone, and Togo (John et al., 2004).

  • West African Transition: Cape Verde Islands, Gambia, Mauritania, and Senegal (John et al., 2004).

  • St Helena and Ascension Islands: St. Helena (John et al., 2004).

  • Laurencia translucida M. T. Fujii et Cordeiro-Marino

  • Type locality: Padres beach, Aracruz, Espírito Santo State, Brazil.

  • Distribution: Warm Temperate Southwesern Atlantic: Brazil: São Paulo (Creed et al., 2010).

  • Tropical Southwestern Atlantic: Brazil: Bahia, Ceará, and Pernambuco Espírito Santo (Fujii et al., 2006), Rio de Janeiro (Creed et al., 2010).

  • Laurencia venusta Yamada

  • Type locality: Koshiki-jima, Kagoshima Prefecture and Goto-retto, Nagasaki Prefecture, Japan.

  • Distribution: Tropical Northwestern Atlantic: México: Quintana Roo (Sentíes & Fujii, 2002).

  • Tropical Southwestern Atlantic: Brazil: Espírito Santo (Fujii & Sentíes, 2005).

Species inquirenda

  • Laurencia alsidiiformis Zanardini ex Fraudenfeld

  • Type locality: Spalato, Dalmatian coast.

  • Laurencia alsidioides P. L. Crouan et H.M. Crouan

  • Type locality: I. Guadeloupe, Caribbean Sea.

  • Laurencia botryocephala Kützing

  • Type locality:“Ad Caput Bonae Spei” Cape of Good Hope.

  • Laurencia canariensis Montagne ex Kützing

  • Remarks: Gil Rodríguez et al. (2012) suggested that it should be considered an uncertain species. According to John et al. (1994), L. canariensis and L. caespitosa are synonyms of Osmundea hybrida (De Candolle) K. W. Nam.

  • Type locality: Canary Islands.

  • Laurencia moriformis Kützing

  • Type locality: Cape of Good Hope.

  • Laurencia trifaria Kützing

  • Type locality: Cape of Good Hope.

PAE Analysis. The area cladogram obtained had the following parameters: Length = 28, Consistency Index=0.85 and Retention Index=0.88. The strict consensus tree of the 3 equally parsimonious trees is presented (Figure 2). Cladogram topology suggests four areas of endemism: South Africa (AghB) with four restricted species, Brazil (EB, NEB, and SEB) with four restricted species, Northeastern Atlantic (WMe, SEAS, LevS, and AdS) with three restricted species, and Gulf of Guinea (SHAI, GGU, CV, GGW, and GGC) with four restricted species (Figure 3). Some of these species, however, are also distributed in the Indo-Pacific (see Table 1). In addition, we have defined three categories of areas: partial congruence (areas with partial congruence between the areas of distribution) composed by GA, ECa, WCa, and SCa (Figure 2), secondary areas (area with an endemic species, Ippi & Flores, 2001) and widespread species (Table 1).

Figure 2 Areas of endemism defined in the PAE analysis. 1) Northwestern At lantic, 2) South Africa, 3) Gulf of Guinea, and 4) Brazil. The black dots represent restricted species or synapomorphies and the white dots represent homoplasies. 

Figure 3 Map of the areas of endemism of Laurencia in the Atlantic Ocean. 

Table 1 Categories of areas defined for Laurencia in the Atlantic Ocean. 

*Species also distributed in the Indo-Pacific. +Species also distributed in the Macaronesian Archipelago.

Discussion

The nomenclature from genus to species, valid names, and taxonomic synonyms of Laurencia are a fundamental part of the checklist here proposed and a topic of continuing discussion among taxonomists. Checklists allow for the documentation of species distributions, the biodiversity within certain areas, and offer the possibility of using this information to carry out a biogeographical analysis; thus, considering the taxonomic remarks, uncertain records, reports of invasion, and in troduction of species allows us to obtain biogeographical natural pat terns or approximate reality. Taxonomic validity of the records and the recognition of the distribution limits of the species area are essential requirements in biogeographic works (Morrone, 2013). In turn, areas of endemism and secondary areas can be defined, and widespread spe cies identified.

On endemism. Areas of endemism (non-endemic species) are defined as the sympatric distribution congruence of two or more taxa belon ging to a given category (e.g., order, family, genus or species) (Morrone, 2013). However, when we take Laurencia, the Caribbean Sea is defined by partial congruence in the distribution of two or more species (group GA, ECa, WCa, and SCa; see Figure 2). Endemic species inhabit this region, such as L. laurahuertana in the western Caribbean, L. foldatsii in the southern Caribbean, L. chondrioides, and L. minuscula in the Caribbean Sea in general, but their distributional congruence is not total, and the PAE analysis does not define this area for two or more synapormor phies. Furthermore, the Caribbean Sea is the Atlantic biotic area with the highest species richness of Laurencia (13 spp). This biogeographic pattern is also shared by the distributional diversity of several unrelated taxa, such as coastal fishes, mangroves, coral reefs, and seagrasses in the Atlantic Ocean (Tittensor et al., 2010).

According to Tapia-Silva et al. (2015), a mathematical analysis of the geographic distribution of the macroalgal species richness can reveal high diversity spots that, in the case of macroalgae, coincide well with the major distribution of the great marine environments in the area (mangroves, coral reefs and seagrasses): the Mexican Caribbean barrier reef, the Veracruz reef system, and the Alacran reef system at Puerto Progreso, Yucatan (Vilchis et al., in press). Studies have shown higher macroalgal diversity in the Indo-Pacific area than in the Atlantic (Kerswell, 2006), and when comparing worldwide Laurencia data (Tapia et al., 2015) this pattern is confirmed. Areas of endemism in the south Atlantic were also found in Brazil, Gulf of Guinea, and South Africa, which are also reported to contain endemic species (Brown & Lomolino, 1998); furthermore, it was found that the Gondwana breakup is the geological process that explains this endemism.

Other areas such as the Northwestern Atlantic, Europe, and the Caribbean Sea share Laurencia species with other regions (i.e., the Indo-Pacific), and the influence of vicariance events such as the closing of Isthmus of Panama and the final closure of the Tethys seaway in the Eastern Atlantic (Cowman & Bellwood, 2013) has not been studied.

Secondary areas. These areas are defined by the presence of one endemic species. When this happens, for example, in the Macaronesian Archipelago with L. viridis, the area is inhabited mostly by species that are also distributed in other places (9 spp.), and the number of endemic species is smaller compared to the defined areas of endemism. In the Macaronesian Archipelago, the phycofloristic composition reveals elements in common with the littoral of continental Europe and the North of Africa (Haroun and Prud’Homme van Reine, 1993; Tuya & Haroun, 2009). This is because the geological origin of the Macaronesian islands dates to the early Miocene (20 my) (Brown & Lomolino, 1998), allowing the colonization of species from other areas. Thus, this region is a spe cial biotic area that could be researched using an island-biogeography approach.

Widespread species. The genus Laurencia in the Atlantic Ocean extends from the coast of Ireland to South Africa, including the Mediterranean Sea and Black Sea; in the western Atlantic, the genus extends from North Carolina, USA, to southern Brazil. Seventeen of these species are also distributed in the Indo-Pacific, of which five are widely distributed in the Atlantic Ocean.

Recent phylogenetic studies have been useful in detecting misidentifications in the Atlantic, especially in records from Macaronesia, Brazil, and the Mexican Caribbean, although only nine widespread species of Laurencia in the Atlantic have a molecular characterization in these places. The use of the molecular-phylogenetic approach on these species in the Atlantic Ocean should allow us to identify new lineages over a wide distribution range, as has happened with other groups of red algae (Skage et al., 2005; Nuñez-Resendiz et al., 2015), and achieve a much better understanding of the historical biogeography of Laurencia in the Atlantic Ocean.

According to Miranda and Marques (2011), the two principal obstacles in the biogeographical works are (1) the reliability of species identifications and the consequent uncertainty of the presence of species in a given area, and (2) the difficulty in producing reliable cladograms from phylogenies.

In conclusion, it has been possible to establish a biogeographic pattern in Laurencia from the definition of areas of endemism and partial and secondary areas. This pattern has been linked to geological events that occurred in the past. Therefore, the recognition of new species from systematics studies and the clarification of taxonomic problems will allow researchers to continue developing a biogeographic hypothesis for the genus in the Atlantic Ocean.

Acknowledgements

The first author wishes to thank the Universidad Autónoma Metropolitana-Iztapalapa and CONACyT. We also thank the following projects: UAMI, Consejo de la Div. C.B.S., (Sesión 15.14-131014) and Secretaría de Educación Pública-PROMEP (UAMI-CA-117), the São Paulo Research Foundation (FAPESP, 2014/00012-1), and CONACyT. Finally, we thank Michael Wynne for his comments on the manuscript.

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Received: May 31, 2017; Accepted: October 30, 2017

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