Conspecificity of two morphologically distinct calcified red algae from the northwest Pacific Ocean: Galaxaura pacifica and G. filamentosa (Galaxauraceae, Rhodophyta)

Liu et al. Botanical Studies 2013, 54:1 http://www.as-botanicalstudies.com/content/54/1/1 RESEARCH Open Access Conspecificity of two morphologically distinct calcified red algae from the northwest Pacific Ocean: Galaxaura pacifica and G. filamentosa (Galaxauraceae, Rhodophyta) Shao-Lun Liu1, Lawrence M Liao2 and Wei-Lung Wang3* Abstract Background: Members of the calcified red algal genus, Galaxaura, are distributed predominantly in warm temperate, subtropical, and tropical regions worldwide. The capacity of these algae to form calcified thalli could play a critical role in the carbon cycle of these ecosystems. Previous studies have suggested that the reported species diversity of Galaxaura may be exaggerated due to a lack of knowledge regarding external morphological differences between gametophytic and tetrasporophytic plants (or among different life stages) of a single species. Results: To examine this issue, this study collected specimens of two morphologically distinct Galaxaura from Taiwan and the Philippines. These specimens were initially identified as two species (G. pacifica Tanaka and G. filamentosa Chou ex Taylor) based on their morphological features. Our molecular analyses, however, unexpectedly showed that these two specimens shared 100% identical rbcL sequences, indicating that they represented a single species comprising two distinct external morphologies. Furthermore, our extensive observations and molecular analyses on several specimens from different locations in southern Taiwan has revealed that these morphological differences could be due to seasonal variation. Conclusions: This study proposes that G. “filamentosa” from the Philippines could represent the remnants of the lower villous part of older gametophytic plants of G. pacifica after senescence of the upper smooth part of the thallus. As such we propose that these two previously distinct algal species from the northwest Pacific Ocean as a single species, G. pacifica. This study shows that the biodiversity of the calcified red algae Galaxaura could be overestimated without the assistance of molecular tools. Additionally, this study provides insights into the biodiversity and unique biology of the calcified red algae Galaxaura. Keywords: G. filamentosa; G. pacifica; Galaxauraceae; rbcL; Rhodophyta; Taiwan; The Philippines Background Species of the calcified red algal family Galaxauraceae are distributed widely throughout the shallow marine waters of the warm temperate, subtropical, and tropical regions (e.g., Littler and Littler, 1997; Abbott 1999; Huisman, 2006). The unique ability of these red algae to incorporate calcium carbonate into their thalli makes them critical elements in the carbon budget, biomineralization, reef * Correspondence: 3 Department of Biology, National Changhua University of Education, Changhua 500, Taiwan Full list of author information is available at the end of the article building processes, and coastal marine ecosystems. Research related to their biodiversity is necessary to understand their contribution to the carbon cycle of tropical marine ecosystems because calcium carbonate deposition in algae is affected by environmental conditions and differs from one species to another (Stanley et al., 2010). Seven genera were historically recognized in the family Galaxauraceae, including Actinotrichia Decaisne, 1842, Galaxaura Lamouroux, 1812, Tricleocarpa Huisman and Borowitzka 1990, Gloiophloea J. Agardh, 1872, Scinaia Bivona-Bernardi, 1822, Nothogenia Montagne, 1843, and Whidbeyella Setchell and Gardner 1903 © 2013 Liu et al.; licensee Springer. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Liu et al. Botanical Studies 2013, 54:1 http://www.as-botanicalstudies.com/content/54/1/1 (reviewed in Huisman, J.M 2006). Huisman et al. (2004a) used molecular analyses to resurrect the genus Dichotomaria Lamarck 1816 from synonymy under Galaxaura, and split the family Galaxauraceae into two different families, Galaxauraceae and Scinaiaceae. The former currently comprises four calcified genera, Actinotrichia, Dichotomaria, Galaxaura, and Tricleocarpa; whereas the latter consists of four non-calcified genera, Gloiophloea, Scinaia, Nothogenia, and Whidbeyella. The genus Galaxaura was first erected by Lamouroux (1812). Kjellman (1900) recognized 62 species and described 47 of these species as new, suggesting that the genus Galaxaura is extremely diverse. However, later studies challenged this taxonomic system. Howe (1917, 1918) suggested that the species diversity of Galaxaura could be inflated because of the different external morphologies in the sexual (i.e., gametophytic) and sporophytic (i.e., tetrasporophytic) stages, referred to as the dimorphic life history (e.g., Wang et al. 2005). Guided by this concept, two fundamental studies that investigated the calcified red algal family Galaxauraceae in the Indian Ocean and Australian region reduced a significant number of different species to a few pantropical species such as Galaxaura rugosa, G. marginata (= Dichotomaria marginata), and G. obtusata (= D. obtusata ) (Papenfuss et al. 1982; Huisman and Borowitzka 1990). The elucidation of a possible relationship between two morphologically different (e.g., gametophytic vs. tetrasporophytic) species of the calcified red algal genus Galaxaura remains largely unexplored, although the concept of the dimorphic life history was only recently proven and the synonymy of some Galaxaura species has been demonstrated (Huisman et al. 2004b; Kurihara et al. 2005; Wang et al. 2005). Wang et al. (2005) suggested that the genus Galaxaura should have more diverse species in the tropical oceans and that the synonymy of numerous species based solely on morphological observations should be reassessed carefully after showing that the monophyly of a pan-tropical species, G. rugosa, was not supported by their molecular analyses. To examine this issue, we collected two specimens of the genus Galaxaura from Taiwan and the Philippines. Based on their morphological characters, the specimens were initially identified as two different species. They were identified according to the taxonomic keys in the literature as Galaxaura pacifica Tanaka (Tanaka, 1935) and G. filamentosa Chou ex Taylor (Chou, 1945). The thallus of G. pacifica comprises a lower villous portion where branches are very hairy (i.e., villous) and composed of numerous assimilatory filaments and an upper smooth portion where branches are very smooth (i.e., glabrous) and lack assimilatory filaments (Tanaka, 1935, 1936). In contrast, the branches of G. filamentosa are extremely villous throughout the thallus (Chou, 1945). Page 2 of 19 Thus, G. pacifica was considered to be in the sexual phase (i.e., gametophytic plants (...truncated)