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Introduction
Isla Guadalupe is a natural reserve that represents a unique ecosystem as other Mexican islands. Its volcanic origin and distance from the Baja California peninsula have allowed for a successful evolutionary development of both its particular land and marine flora and fauna, as can be inferred by the high number of cases of endemism recorded (Aguirre-Muñoz et al., 2003; García-Gutiérrez et al., 2005). However, studies on biodiversity, particularly of marine life, are lacking for Isla Guadalupe, mainly because of the difficulty to access the island. The available studies on marine flora of Isla Guadalupe date back to the late 1800s and were published by Setchell and Gardner (1930) in a list that included 90 species of macroalgae. The last review of the macroalgae of Isla Guadalupe was carried out by Stewart and Stewart (1984) and included 212 species, with 24 new records. Both studies recorded a large number of genera of subtropical affinity, indicating that the marine flora in the island is more characteristic of a subtropical than a temperate environment.
The difficulty in accessing an area such as Isla Guadalupe to carry out scientific research is the main cause that many marine communities are yet to be studied, even in their most basic aspects such as species composition. Thus, no published work existed hitherto on diatoms from that area, nor planktonic or benthic forms, in spite of being the most diverse, abundant and productive algal group in marine ecosystems.
In general, studies on benthic diatoms from the Mexican NW are scarce, and these are related either with their role in the feeding habits of abalone (Haliotis spp.) and grazing intertidal molluscs (Siqueiros-Beltrones & Valenzuela-Romero, 2004), or the structure of epiphytic forms assemblages found on macroalgae and marine plants (Argumedo-Hernández & Siqueiros-Beltrones, 2008; Siqueiros-Beltrones, Serviere-Zaragoza, & Argumedo-Hernández, 2002). Another study describes assemblages of epipelic diatoms characteristic of mangrove environments (López-Fuerte, Siqueiros-Beltrones, & Navarro, 2010).
In this study we begin the construction of a taxonomic basis that serves for monitoring and assessing the environmental health of any ecosystem, and provide the first floristic account of benthic diatoms from Isla Guadalupe.
Materials and methods
Isla Guadalupe is located in the Mexican Pacific Ocean approximately 256 km off the coast of the Baja California peninsula at 29° N, 118° W, within the Guadalupe Island Biosphere Reserve (Fig. 1). It is influenced by the California Current which is characterized by low temperature and salinity (Lynn & Simpson, 1987). Surficial water temperature ranges between 15 and 20 °C during winter and between 20 and 22 °C in summer. Its ocean volcanic nature and its remote distance from the coast confer it an abrupt topography and a unique biodiversity. The coastal zone physiography consists of loose basalts, blocks, dikes, cliffs, and few sandy beaches (Pierson, 1987).
Sample collection
Surficial temperature, salinity and pH were measured in situ using a field multi-sensor (Horiba U10). Benthic diatoms were collected at Guadalupe Island in one sampling site on January 18, 2013. Epiphytic diatoms were scraped off from specimens of Eisenia desmarestioides Setchell and N.L. Gardner, 1930 (Ochrophyta; Laminariales), and Codium latum subsp. palmeri (E.Y. Dawson) P.C. Silva, 1962 (Chlorophyta; Bryopsidales), using a glass slide for each sampling. Epilithic and epizoic diatoms from the shell of the sea-snail Megastraea undosa W. Wood, 1828 were brushed off from an area of 5 cm2 in each substrate using a toothbrush. Afterwards, a compound sample was formed for the site and preserved in commercial ethanol (70%); concomitant observations of fresh diatom samples were made. In order to clean the diatom frustules for identification the organic matter was oxidized with a mixture of sample, commercial ethanol and nitric acid at a 1:3:5 proportion (Siqueiros-Beltrones, 2002). The samples were then rinsed with drinking water until reaching a pH >6. From each compound sample three permanent slides were mounted for each substrate using Zrax(r) (RI: 1.7) as mounting medium. All species names and authorities were revised, and in certain cases nomenclatural updates were made, confirming all of the currently accepted taxonomic names. In order to revise the taxonomic names and their synonymies, we consulted Round, Crawford, and Mann (1990) along with the data bases on www.algaebase.org (Guiry & Guiry, 2014) and www.marinespecies.org (WoRMS Editorial Board, 2014). Taxonomic keys used for species identification included: Schmidt et al. (1874-1959), Peragallo and Peragallo (1897-1908), Foged (1984), Witkowski, Lange-Bertalot, and Metzeltin (2000), Siqueiros-Beltrones (2002), and López-Fuerte et al. (2010). Photographic images of newly recorded taxa and others were acquired using an electronic ocular lens.
Results
Surficial water temperature in the sampling site was measured at 17.7 °C; salinity was recorded at 38 psu, which renders the environment as polyhalobous. The measured pH was close to neutral at 7.4.
Floristic analysis yielded 119 taxa including species and varieties of benthic diatoms, including epiphytic, epilithic and epizoic forms (Appendix). All diatoms appear alive in the fresh mountings (Fig. 2). The class Bacillariophyceae with 87 taxa was much more diverse than the Fragilariophyceae which yielded 32 taxa. Out of the 45 identified genera, those with higher number of species were Mastogloia (13), Diploneis (11 species), Nitzschia (10), Cocconeis (9), Grammatophora (6) and Licmophora (5). These represent 46% of the species recorded in this study. In contrast, 25 genera were represented by a single species. Thirteen taxa are new records for Mexico: Achnanthes citronella (A. Mann) Hustedt (Fig. 40), Amphiprora conspicua Greville (Fig. 18), Amphora proteus var. oculata H. Peragallo (Fig. 41), Campylodiscus ambiguus Greville (Fig. 3), Diploneis coffaeiformis (Schmidt) Cleve (Fig. 34), D. suborbicularis var. constricta Hustedt (Fig. 33), Donkinia reticulata Norm. (Fig. 35), Lyrella perplexoides (Hustedt) D.G. Mann (Fig. 39), Mastogloia asperuloides Hustedt (Fig. 43), M . ciskeiensis Giffen (Figs. 38 and 42), M . punctatissima (Greville) Ricard (Fig. 44), Parlibellus delognei (Van Heurck) E. J. Cox (Fig. 37) and Psammodiscus calceatus T. Watanabe, T. Nagumo and J. Tanaka (Fig. 31). Only 11 taxa occurred in all three surveyed substrates. The higher number of taxa was observed on the rocky substrate (57), and the lowest on the shell of Megastraea undosa . On the other hand, the higher number of exclusive taxa occurred on macroalgal substrate, particularly on Eisenia desmarestioides with 29 taxa, which renders it as a proper substrate for diatoms, while M . undosa had the lowest (6) number of taxa.
Figures 2-9 Iconographic sample of the diatoms observed on different coastal substrata from Isla Guadalupe. All images by Folf. Bar=10μm. (2) Campylodiscus crebrecostatus var. speciosa, (3) Campylodiscus ambiguus, (4) Campylodiscus fastuosus, (5) Podocystis adriatica, (6) Campyloneis grevillei, (7) Lyrella approximata, (8) Mastogloia fimbriata, (9) Surirella fastuosa.
Figures 10-19 10) Girdle view, (11) Rhabdonema adriaticum, (12 and 13) Rhabdonema arcuatum, (14) Diploneis bombus, (15) Girdle view, (16) Climacosphenia moniligera, (17) Alveus marinus, (18) Amphiprora conspicua, (19) Gephyria media.
Figures 20-34 (20) Licmophora abbreviata, (21) Grammatophora marina, (22) Grammatophora undulata, (23) Campylopyxis garkeana, (24) Trachyneis aspera, (25) Brachysira aff. neoexilis, (26) Denticula kuetzingii, (27) Plagiodiscus nervatus, (28) Licmophora communis, (29) Licmophora ehrenbergii, (30) Licmosoma squamosum, (31) Psammodiscus calceatus, (32) Cocconeis molesta var. crucifera, (33) Diploneis suborbicularis var. constricta, (34) Diploneis coffaeiformis.
Discussion
Research on benthic marine diatoms in Mexico dates barely to the 1980s, and most studies have been carried out for the NW region. Recently, however, some have been carried out in the Mexican Caribbean area (Hernández-Almeida, Herrera-Silveira, & Merino-Virgilio, 2013; López-Fuerte, Siqueiros-Beltrones, & Hernández-Almeida, 2013; Siqueiros-Beltrones, Argumedo-Hernández, & Hernández-Almeida, 2013). Nonetheless, there are still extensive areas in the country where the most basic floristic studies on benthic diatoms are lacking and are badly needed.
Our present work falls within this category, inasmuch no research on diatoms, whether scientific or of any sort, existed for Mexican islands, in spite the fact that 1365 islands are distributed within the Mexican territory (Comité Asesor Nacional sobre el Territorio Insular Mexicano, 2012). Thus, this constitutes the first floristic list of benthic diatoms for any oceanic island located in the exclusive economic zone of Mexico, and it targets the Guadalupe Island Biosphere Reserve.
Although only three substrates were examined, the number of identified taxa is high, and over 11% are new records for the whole country. Some of the genera with a higher number of species are of tropical affinity, e.g., Mastogloia . Others such as Cocconeis thalassiana , primarily described for the Mexican Caribbean (Romero & López-Fuerte, 2013), leads us to suggest that, as with the terrestrial flora, Isla Guadalupe does not have a diatom flora with a particular bio-geographical affinity, i.e., temperate, subtropical, or tropical. Moreover, due to the distance of the island with the continent it is likely that further observations based on a more exhaustive sampling may render new records of diatom species or varieties. This, and on the basis that Isla Guadalupe is not influenced by coastal upwelling, shows a biogeographically mixed macroalgal flora that includes species from California, the Mexican tropics, and the insular Indo-Pacific, plus a conspicuous group of endemic taxa derived from the California flora. All of these are evidence of their effective isolation and the ecological divergence in a process of speciation (Dawson, 1960).
In comparison with E. desmarestioides that stands out as a proper substrate for diatoms with 29 exclusive taxa and the second most number of taxa overall, Siqueiros-Beltrones et al. (2002) did not find diatom epiphytes on Eisenia arborea Areschoug, although recent research has shown that older blades may harbor monospecific proliferations of diatoms. Along the West coast of the Baja California Peninsula, Macrocystis pyrifera (Linnaeus) C. Agardh is considered the main food source of abalone (Haliotis spp.), together with its numerous epiphytic diatom species (Argumedo-Hernández & Siqueiros-Beltrones, 2008). However, in Isla Guadalupe M. pyrifera is absent, thus its ecological role may be replaced by E. desmarestioides , which is the largest macroalgae in the area and, according to the local fishermen, its abundance relate to the that of abalone.
Aside from this being the first publication on the diatom flora of Isla Guadalupe or any other Mexican island, the high number of new records either for the region or the whole country gives an insight to a highly diverse flora hitherto unknown as an assemblage. Thus, the generated information is relevant both in bio-geographical as well as in environmental health terms. We are confident that further exhaustive research will provide much valuable information that is hard to come by, given the remoteness of the studied area. The differential distribution of exclusive diatom taxa on distinct substrates strongly supports the expectation of increasing the species richness for the island as more substrates are examined.
