Accessible Published by De Gruyter August 31, 2020

The Ulvophyceae (Chlorophyta) of eastern Sorsogon, Philippines, including Halimeda magnicuneata sp. nov. (Bryopsidales)

Richard V. Dumilag ORCID logo, Ferdinand S. Dumago, Rea Kissel R. Cabudoy, Mark Christian E. Peralta, Camille C. Li, Glenn Cedrick V. Gamus, Rose Glendelyn T. Romero, Sandra L. Yap, Michael Y. Roleda, Paul John L. Geraldino, Heroen Verbruggen, Frederik Leliaert, Stefano G.A. Draisma, Lawrence M. Liao and Gerald T. Kraft
From the journal Botanica Marina

Abstract

The marine algal flora of eastern Sorsogon has been intensively collected and is generally considered as the richest in the Philippines. A trend of species records in the area has been dominated by rhodophytes (red algae) with significantly fewer similar studies for other algal groups (green and brown algae). In this study we present an updated catalogue of the green seaweeds (Ulvophyceae) of eastern Sorsogon. A checklist, including notes on taxonomy, is given of the 103 species. Twenty-six species are newly recorded locally of which five represent new records for the Philippines: Avrainvillea amadelpha, Caulerpa buginensis, an unidentified Caulerpa species, Codium cf. latum, and one taxon new to science. The new species is described as Halimeda magnicuneata Verbruggen et Dumilag based on morpho-anatomy and DNA sequence data. The number of ulvophycean species recorded in eastern Sorsogon is found to be the highest in the Philippines. This may be a result of the high collection effort in the region, as well as eastern Sorsogon’s diverse habitats providing favourable conditions for a wide range of seaweed species.

1 Introduction

Sorsogon province (Figure 1) is located at the southeasternmost tip of Luzon Island, Philippines. The area intercepts the latitudes between 12°75′N and 13°02′N and longitudes at 123°E to 124°E. Sorsogon rims the southernmost border of peninsular Bicol, an allochthonous oceanic island which drifted northwards until its amalgamation unto the southeastern edge of greater Luzon Island, about 45 million years ago (Hall 1997 2002). Its eastern region straddles the embayment along the shallow San Bernardino Strait, an expanse that receives the offshoots of the nutrient-rich waters of the North Equatorial Current (NEC) from the Pacific basin, before its diversion into the Visayan seas (Gordon et al. 2011). Although not rigorously tested, the geographical location of eastern Sorsogon, together with its complex paleogeographical history, climate, and coastal physiography, contributes to its abounding marine biodiversity. The seafloor of eastern Sorsogon is primarily composed of volcanic basalt where extensive biogeochemical activities allow the hosting of a more diverse algal flora than in places with coral or calcareous substrata (Kraft, personal observation). Claims about the seaweed diversity in this area being the richest and most varied in the Philippines (Kraft et al. 1999; Trono 1975) have gone largely unchallenged. For more than five decades, the area has received continued attention from many phycologists around the world, including those studying the local flora (e.g., Dumilag et al. 2014, 2018; Kraft 1969; Kraft et al. 1999; Trono 1975 1976) and the taxonomy or biogeography of tropical taxa (e.g., Boo et al. 2016; Gabriel et al. 2017; Payo et al. 2013; Santiañez et al. 2018; Wiriyadamrikul et al. 2013).

Figure 1: Collecting sites (abbreviations as used in main text in brackets) in eastern Sorsogon. The inset indicates the location of Sorsogon within the Philippines.

Figure 1:

Collecting sites (abbreviations as used in main text in brackets) in eastern Sorsogon. The inset indicates the location of Sorsogon within the Philippines.

The town of Bulusan, situated at the mid-eastern point of Sorsogon, is one of the long-time favourite collecting sites in the province, if not the entire Philippines. Specimens collected from this area formed the basis for the description of seven new species, namely Cubiculosporum koronicarpis Kraft (Kraft 1973), Ptilophora scalaramosa (Kraft) R.E.Norris (Norris 1987), Rhipiliopsis carolyniae Kraft (Kraft 1986a), Corynocystis prostrata Kraft (Kraft et al. 1999), and Betaphycus philippinensis Doty (Doty 1995), now relegated to synonymy under Betaphycus gelatinus (Esper) Doty ex P.C.Silva (Dumilag 2018), and Halymenia tondoana O.DeClerck et Hernández-Kantún (Hernández-Kantún et al. 2012), as well as one subspecific taxon, Eucheuma arnoldii var. alcyonida Kraft (Kraft 1972), now Mimica arnoldii var. alcyonida (Kraft) Santiañez et M.J.Wynne (Santiañez and Wynne 2020).

Initial documentation of seaweeds in southeastern Sorsogon was stimulated in part by an interest in its potentially exploitable resources (Kraft 1969; Taylor 1977), with some progress being made to understand the seaweed composition and diversity of the area (De Smedt et al. 2001; Kraft et al. 1999; Rollon et al. 2003; Trono 1972, 1975, 1976). Although most of the new species and records from eastern Sorsogon to date have centered on the Rhodophyta, particularly in Bulusan, the entire region is additionally well endowed with green and brown algae. The object of our present report turns to the green macroalgae, collectively regarded as belonging to the Ulvophyceae, a class representing an extraordinary diversity particularly in tropical and warm-temperate waters (Huisman and Saunders 2007). More than 1900 species are included in the class (Guiry and Guiry 2020), which are distributed in marine and brackish habitats around the world. A relatively smaller diversity (ca. 200 species) is also found in freshwater and terrestrial habitats, mainly known from temperate regions, but is likely much higher in tropical areas (Škaloud et al. 2018). Many ulvophyceans are of economic importance, among them are several species of Caulerpa such as Caulerpa chemnitzia (Esper) J.V.Lamouroux, Caulerpa lentillifera J.Agardh, and Caulerpa racemosa (Forsskål) J.Agardh that are widely consumed in the Indo-Pacific region (Gaillande et al. 2017). The aquaculture of Ulva spp. has aroused considerable interest lately because of its species’ potential in mitigating major environmental impacts faced by marine food production systems (Bolton et al. 2016), e.g., coastal eutrophication due to extensive fish culture (Roleda and Hurd 2019). Other ulvoids have been suggested to be rich sources of pharmacologically active compounds (see Güven et al. 2010; Smith 2004).

Published and herbarium-specimen information on Ulvophyceae reported from eastern Sorsogon can be difficult to find, because most available information is dated, published in journals (e.g., Belleza and Liao 2007; Trono 1972a, 1975) or books (e.g., Trono 1997, 2004, 2017, 2018) of limited distribution or in the form of unpublished notes (e.g., Kraft 1969). No comprehensive work that compiles all the records of Ulvophyceae in eastern Sorsogon has been published, and it is only those studies by Trono (1972a 1975) that incorporate reliable species documentation of the Ulvophyceae. The aim of this study is to provide a comprehensive checklist of ulvophycean species occurring in eastern Sorsogon, Philippines, including taxonomic notes on the species. During the survey of herbarium specimens, we also examined a species of Halimeda that was previously recognised as new to science based on DNA sequence data (Verbruggen et al. 2009) but not yet formally described. We provide the species description in the present study.

2 Materials and methods

We bring together available data of ulvophycean species collected from eastern Sorsogon from peer-reviewed journal articles and books, open-access databases, and unpublished records from our own sampling conducted in recent years. Specimens were collected by hand during intertidal walks, wading or snorkeling in visited field sites. The collections were identified based on morphology and (where applicable) internal anatomy. For some specimens DNA barcodes were obtained in the framework of previous studies. Scientific names reported from old literature were updated with their current names and synonymies based on AlgaeBase (Guiry and Guiry 2020). For brevity, we hereafter refer to collection sites by abbreviations whenever they occur within particular areas (see Figure 1). The order of species presentation followed the taxonomic arrangement presented by Huisman (2015): Ulvales, Cladophorales, Bryopsidales, Dasycladales and subsequently by family and genus in alphabetical order. The recent proposal by Cremen et al. (2019) to merge the Rhipiliaceae and Udoteaceae with the Halimedaceae was applied.

Various herbaria and collections which house material referred to in this study include BR (formerly lodged at GENT), CEBU, FEUH, HO (specimens are in the process of being transferred from Kraft Herbarium), MICH, MSI, and NCU. Herbarium abbreviations follow Thiers (2020). Ancillary collections, usually in the form of fragments from each voucher specimen preserved in alcohol or silica gel (at least those from CEBU, FEUH and BR), have been stockpiled for future molecular analyses.

Eight major sampling sites in eastern Sorsogon were surveyed to collect samples of Ulvophyceae (Table 1). The total number of recorded species from each site was compared pairwise using Sørensen’s similarity index (Sørensen 1948). The same index modified by Magurran (1988) was used to compare the species diversity in eastern Sorsogon with other regions in the Philippines.

Table 1:

Geographical coordinates and description for the eight study sites surveyed in this study.

Site (abbreviation) Specific collection site(s) Coordinates Description
Prieto Diaz (PD) Brgy. Poblacion 13°02′33″ N, 124°12′0″ E Tide flat is bedrock covered with coarse sand. Chlorophytes are dominated by Bryopsidales and Dasycladales. Ochrophytes are dominated by Fucales and Dictyotales. A few rhodophytes primarily Corallinales are scattered around while Gelidiella acerosa (Forsskål) J.Feldmann et G.Hamel was found throughout the area.
Gubat (GU) Rizal beach 12°53′42″ N, 124°08′11″ E Intertidal area to the east of popular Rizal Beach, composed of shallow-water coral rubble and sand, interspersed with seagrass.
Barcelona (BA) Barcelona Channel 12°52′05″ N, 124°09′05″ E Tide flat is bedrock covered with coarse sand and rocks. Chlorophytes are dominated by Bryopsidales. Ochrophytes are found in the deeper portion of the reef dominated by Turbinaria ornata (Turner) J.Agardh. Rhodophytes found throughout the transect are primarily Corallinales and G. acerosa.
Bulusan (BU) In front of Villa Celeste Resort, Brgy. Dancalan 12°46′00″ N, 124°08′20″ E Upper intertidal flat is bedrock with coral rubble. From 10-100 m the hard substrate is covered with coarse sand and rubble with seagrasses. Co-occurring seaweeds are dominated by Bryopsidales (Caulerpa, Halimeda, Udotea and Avrainvillea). Ochrophytes are dominated by Fucales (Sargassum, Turbinaria and Hormophysa). A few rhodophytes observed are primarily Corallinales.
Brgy. Dapdap 12°45′10″ N, 124°08′27″ E Vast intertidal area adjacent to town proper marked by wide sandbars which join seaward with tracts of reef tops surrounding some deep interconnected lagoons. Gelidioids and eucheumatoids dominate the reef flats, with larger foliose rhodophytes and green algae found on lagoon walls where surge channels provide vigorous water exchanges.
San Bernardino Is. 12°45′07″ N, 124°16′56″ E Basaltic rocky island on the northern entrance of San Bernardino Strait, 16 km east of Bulusan town proper. Sampling done at west and southwest leeward sides, marked by shallow surge channels with sandy bottom perpendicular to the coast. Dense Sargassum beds with numerous understorey red algae, with Chnoospora minima (Hering) Papenfuss forming a belt on the shallowest reaches.
Sta. Magdalena (SM) Olango Beach 12°39′17″ N, 124°07′23″ E A flat consisting of white coarse sand, dominated by seagrasses with some boomies and coral rubble scattered all around. This area completely exposed during low tide. Strong waves are observed during monsoon season. Toward the end of the flat is a mixture of Sargassum patches and live corals.
Brgy. San Rafael 12°39′36″ N, 124°07′52″ E A semi-enclosed bay, with generally a similar physiognomy as Olango Beach. The first 30–40 m has sandy-rocky bottom dominated by a mixture of seagrasses and green seaweeds, viz. members of Siphonocladaceae and Dasycladales. Particularly during low tide, strong waves battered reef edges causing surf splashes.
Matnog (MT) Brgy. Tabunan 12°34′39″ N, 124°05′33″ E Narrow intertidal ca. 600 m southwest of ferry port. Sandy to rocky substrate with dense seagrass patches on reef before drop off ca. 180 m from the coast.
Tikling Is. (TI) East side of Tikling Is. 12°35′02″ N, 124°07′41″ E Island with coarse sandy and rocky shoreline. Substrate within the 100 m transect is predominantly coarse sandy rocky with coral rubble. Chlorophytes are dominated by Dasycladales and Bryopsidales while Ulvales was found throughout the transect. Rhodophytes primarily belong to Gigartinales.
Juac Is. (JI) North east side of Juac Is. 12°33′18″ N, 124°07′11″ E Island with rocky shoreline. The intertidal and reef flat littered with coral rubble from the shore up to 50 m distance. Dominant seaweed species belong to Gigartinales and Dasycladales. The upper subtidal from 60 to 100 m, diverse seaweed flora are associated with live corals, with patches of dense Caulerpa racemosa cover.

3 Results

The species checklist of Ulvophyceae recorded in eastern Sorsogon, Philippines, is presented in Table 2 with notes as appropriate. A comprehensive reference of previous records in the area and a list of citations per site of all exsiccatae examined in this study are provided in Supplementary Table S1.

Table 2:

Checklist and distribution of species of Ulvophyceae recorded from eastern Sorsogon, Philippines with some notes on selected taxa.

Note Taxona Eastern Sorsogon site
PD GU BA BU SM MT TI JI
Ulvales
 Ulvaceae
  Ulva australis Areschoug + + ±
  Ulva clathrata (Roth) C.Agardh ±
  Ulva flexuosa Wulfen + +
  Ulva intestinalis Linnaeus ±
  Ulva kylinii (Bliding) H.S.Hayden, Blomster, Maggs,
   P.C.Silva, Stanhope et Waaland + ±
  Ulva lactuca Linnaeus + + + ± ± ±
  Ulva reticulata Forsskål + + + + ± + ±
Cladophorales
 Anadyomenaceae
  Anadyomene plicata C.Agardh + + ± +
  Microdictyon cf. umbilicatum (Velley) Zanardinib +
  Microdictyon okamurae Setchell + +
1  Boodleaceae
  Boodlea coacta (Dickie) G.Murray et De Tonib +
  Boodlea composita (Harvey) F.Brand ± + ± + ±
  Cladophoropsis vaucheriiformis (Areschoug) Papenfuss + +
  Phyllodictyon anastomosans (Harvey) Kraft et M.J.Wynne + +
2   Struvea okamurae Leliaert + +
 Cladophoraceae
  Chaetomorpha antennina (Bory) Kützing + + ± + +
3   Chaetomorpha vieillardii (Kützing) M.J.Wynne + + + +
  Cladophora aokii Yamada +
4   Cladophora quisumbingii Manza ± ±
5   Cladophora vagabunda (Linnaeus) Hoekb +
  Lychaete dotyana (W.J.Gilbert) M.J.Wynne + +
 Dictyosphaeriaceae
  Dictyosphaeria cavernosa (Forsskål) Børgesen + + ± +
  Dictyosphaeria versluysii Weber Bosse + + ± ± +
 Siphonocladaceae
  Boergesenia forbesii (Harvey) Feldmann + + + + ± + +
  Valoniaceae
  Valonia aegagropila C.Agardh + + ± + +
  Valonia fastigiata Harvey ex J.Agardhb + +
  Valonia utricularis (Roth) C.Agardh +
  Valonia ventricosa J.Agardh + ± +
  Valoniopsis pachynema (G.Martens) Børgesen ± +
Bryopsidales
 Bryopsidaceae
6   Bryopsis pennata J.V.Lamouroux + + + +
 Caulerpaceae
  Caulerpa ambigua Okamurab
7   Caulerpa biserrulata Sonderb + +
  Caulerpa brachypus Harvey +
8   Caulerpa buginensis E.Verheij et Prud’hommeb, c +
  Caulerpa chemnitzia (Esper) J.V.Lamouroux + + + +
  Caulerpa cupressoides (Vahl) C.Agardh + + + +
9   Caulerpa elongata Weber Bosse + + +
  Caulerpa fergusonii G.Murray + +
10   Caulerpa filicoides Yamada ±
  Caulerpa lentillifera J.Agardh + + + ± + ±
  Caulerpa lessonii Bory + + +
  Caulerpa mexicana Sonder ex Kützing +
  Caulerpa opposita Coppejans et Meineszb +
Caulerpa pickeringii Harvey et Bailey  +
  Caulerpa racemosa (Forsskål) J.Agardh + + + + + +
  Caulerpa serrulata (Forsskål) J.Agardh ± + + + + +
  Caulerpa sertularioides (S.G.Gmelin) M.Howe + + + + + +
  Caulerpa taxifolia (M.Vahl) C.Agardh + + + +
  Caulerpa urvilleana Montagne ± ± ±
11   Caulerpa sp.b, c, d +
 Codiaceae
  Codium arabicum Kützing +
  Codium bartlettii C.K.Tseng et W.J.Gilbert + + + +
  Codium edule P.C.Silva + + + +
  Codium geppiorum O.C.Schmidtb +
12   Codium cf. latum Suringarb, c, d +
  Codium platyclados R.Jones et Kraft + +
13   Codium cf. tenue Kützing + +
 Dichotomosiphonaceae
14   Avrainvillea amadelpha (Montagne) A.Gepp et E.S.Geppb, c +
  Avrainvillea erecta (Berkeley) A.Gepp et E.S.Gepp + +
  Avrainvillea lacerata J.Agardh + + + ± + +
  Avrainvillea longicaulis (Kützing) G.Murray et Boodle ±
  Avrainvillea nigricans Decaisne ± +
  Avrainvillea obscura (C.Agardh) J.Agardh + +
 Halimedaceae
  Chlorodesmis fastigiata (C.Agardh) S.C.Ducker + + + +
  Halimeda bikinensis W.R.Taylorb +
15   Halimeda borneensis W.R.Taylor ± ±
  Halimeda cylindracea Decaisne + + +
16   Halimeda discoidea Decaisne + + + +
17   Halimeda distorta (Yamada) Hillis-Colinvaux +
  Halimeda fragilis W.R.Taylorb + +
18   Halimeda gigas W.R.Taylor + + + +
19   Halimeda gracilis Harvey ex J.Agardh + +
  Halimeda incrassata (J.Ellis) J.V.Lamourouxb +
  Halimeda lacunalis W.R.Taylorb +
  Halimeda macroloba Decaisne + ±
20   Halimeda macrophysa Askenasy + +
  Halimeda magnicuneata Verbruggen et Dumilag sp. nov. +
21   Halimeda melanesica Valet +
22   Halimeda minima (W.R.Taylor) Hillis-Colinvaux + +
  Halimeda opuntia (Linnaeus) J.V.Lamouroux + ± + + ± + +
  Halimeda taenicola W.R.Taylor ±
23   Halimeda velasquezii W.R.Taylor + + + ± +
  Rhipidosiphon javensis Montagne +
24   Rhipilia crassa A.J.K.Millar et Kraft ±
25   Rhipilia nigrescens Coppejans et Prud’homme +
26   Rhipilia orientalis A.Gepp et E.S.Gepp +
27   Rhipiliopsis carolyniae Kraft +
  Tydemania expeditionis Weber Bosse + + +
  Udotea argentea Zanardinib +
  Udotea indica A.Gepp et E.S.Geppb +
  Udotea occidentalis A.Gepp et E.S.Gepp +
  Udotea orientalis A.Gepp et E.S.Gepp + + + +
Dasycladales
 Dasycladaceae
  Bornetella nitida Munier-Chalmas ex Sonder + + + + +
  Bornetella oligospora Solms-Laubachb +
  Bornetella sphaerica (Zanardini) Solms-Laubach + + + ± +
  Neomeris annulata Dickieb +
  Neomeris vanbosseae M.Howeb + + +
  Halicoryne wrightii Harvey + +
 Polyphysaceae
  Acetabularia dentata Solms-Laubachb + +
  Acetabularia major G.Martens +
  Acetabularia ryukyuensis Okamura et Yamadab +
  Parvocaulis exiguus (Solms-Laubach) S.Berger, Fettweiss,
   Gleissberg, Liddle, U.Richter, Sawitzky et Zuccarellob + +
  Parvocaulis parvulus (Solms-Laubach) S.Berger, Fettweiss, + +
   Gleissberg, Liddle, U.Richter, Sawitzky et Zuccarellob

    PD: Prieto Diaz, GU: Gubat, BA: Barcelona, BU: Bulusan, SM: Sta. Magdalena, MT: Matnog, TI: Tikling Is., JI: Juac Is. (see Table 1).

    “+”, taxon with actual specimen examined in this study; “±” material cited from literature.

    1. Most Philippine specimens, though no representative was collected from Sorsogon, identified morphologically as Boodlea montagnei (Harvey ex J.E.Gray) Egerod, Boodlea siamensis (now B. composita), and Phyllodictyon anastomosans belong to “Boodlea sp. 10”, a widespread Indo-Pacific species (Leliaert et al. 2009).

    2. Phylogenetic inferences from partial LSU and ITS sequences including a specimen (HEC12301) collected from BU indicated that Chamaedoris orientalis Okamura et Higashi should be recognised as a species of Struvea (Leliaert et al. 2007). Due to the peculiar phenotypic traits of S. okamurae relative to other traditionally known members of Struvea, the description of the genus was emended in Leliaert et al. (2007).

    3. Wynne (2011) proposed the name C. vieillardii to serve for what was previously known in tropical seas as Chaetomorpha crassa (C.Agardh) Kützing.

    4. Cladophora quisumbingii has been applied to a species only known from the Philippines. This species was briefly described by Manza (1939) based on an unnumbered specimen collected by R. C. McGregor from Batan Island, Batanes, northern Philippines, dated June 1907. Cladophora quisumbingii exhibits branches arranged dichotomously at the base, becoming di-tetrachotomous at midregion and tapered to narrow apical divaricate ends. Its main axes measured 300–400 µm while the apical branches were 150–200 µm, making this taxon relatively coarse as compared with most Cladophora species. Manza’s description did not include any illustrations. The original material was deposited at the Herbarium of Bureau of Science in Manila but lost at the beginning of World War II. Silva et al. (1987) argues that a specimen in Berkeley (UC 1402218) is the lectotype. The first illustration for this species is provided by Trono (2018).

    5. Cladophora vagabunda is a species-complex that is widespread from tropical to temperate waters (Boedeker et al. 2016). Tropical representatives are genetically distinct from temperate C. vagabunda (type from England) and likely represent a different species.

    6. A preliminary molecular phylogenetic analysis in Bryopsis showed considerable conflict between morphological and phylogenetic species definitions (Hollants et al. 2013). A Philippine specimen identified as B. pennata was found to belong to ‘Bryopsis sp. 28′, a pantropical clade including a wide morphological diversity.

    7. The morphological entity Caulerpa biserrulata represents at least two distinct species and one of those is C. brachypus. The C. brachypus specimen from Cangaluyan Is., Pangasinan, Philippines in Famà et al. (2002) was re-examined and identified as C. biserrulata (Wynne et al. 2009). Nonetheless, it belongs to a clade with typical C. brachypus.

    8. On MICH 679831 (Kraft #359) there are four mounted specimens with pallid coloured thalli with quite distinctive oppositely arranged rounded ramuli. At the bottom of the sheet was handwritten by H. Ohba in pencil, dated 29 May 1998, “Coppejans and Prud’homme van Reine’s new species from Indonesia or Papua New Guinea”. The species to which Ohba was referring is C. buginensis.

    9. The definitive taxonomic traits for C. webbiana have been shown to overlap with C. elongata. This has been seen particularly among Philippine samples (Dumilag et al. 2019), thus molecular confirmation is recommended.

    10. Caulerpa filicoides generally has 2–3 super-imposed whorls on a longer stipe, i.e. 5–15 mm, while another related Indo-Pacific species, Caulerpa andamanensis (W.R.Taylor) Draisma, Prud’homme et Sauvage has a single whorl of branchlets on a short stipe, i.e. up to 2 mm (Draisma et al. 2014). Trono (2018) described his material from BU following the former criterion.

    11. Refer to the Discussion section.

    12. Refer to the Discussion section.

    13. Huisman (2015) noted that reported specimens under the name Codium tenue from the Philippines and the Marshall Islands probably belong to different species and require molecular confirmation.

    14. Refer to the Discussion section.

    15. Record of Halimeda simulans M.Howe in Trono (1975, 1997) was considered by Huisman (2015) to be H. borneensis.

    16. Verbruggen et al. (2005) reported specimens matching Halimeda cuneata f. digitata E.S.Barton from several places in the Philippines, but when sequenced these clearly belong within H. discoidea. Voucher HV827 collected from BU was confirmed molecularly by Verbruggen et al. (2005).

    17. Voucher HV767 from BU was confirmed molecularly by Verbruggen et al. (2009).

    18. Most samples identified as H. tuna in the Indo-Pacific are small plants of H. gigas. The presence of H. tuna anywhere in the Philippines, therefore, is unlikely, as this species occurs only in the Mediterranean and another cryptic species in the Atlantic (Kooistra et al. 2002, Dijoux et al. 2012). The voucher HV769 from BU was confirmed molecularly by Verbruggen et al. (2009) as H. gigas.

    19. Voucher HV824 from BU was confirmed molecularly by Verbruggen et al. (2009).

    20. Voucher HV822 from BU was confirmed molecularly by Verbruggen et al. (2009).

    21. Vouchers HV790 and HV818 from BU were confirmed molecularly by Verbruggen et al. (2005).

    22. Halimeda copiosa Goreau et E.A.Graham is strictly an Atlantic species. Indo-Pacific samples identified as H. copiosa were molecularly assigned to the H. minima complex, which has not been found outside the Indo-Pacific. Voucher HV791 from BU was confirmed molecularly by Verbruggen et al. (2009).

    23. Vouchers HV68 and HV779 from BU were confirmed molecularly by Verbruggen et al. (2009).

    24. A single specimen, NSW419105, collected from BU, was regarded as one of the syntype specimens of this species by Millar and Kraft (2001).

    25. Molecularly confirmed by Verbruggen et al. (2009) from BU.

    26. Molecularly confirmed by Verbruggen et al. (2009) from BU.

    27. The type specimen (MELU, K492), was collected from BU (Kraft 1986).

    aDetailed specimen information presented in Supplementary Table S1.

    bNew record for eastern Sorsogon, Philippines.

    cNew record for the Philippines.

    dNew record for southeast Asian waters.

Twenty-six species are recorded for the first time in the area. Avrainvillea amadelpha (Montagne) A.Gepp et E.S.Gepp, Caulerpa buginensis E.Verheij et Prud’homme and an unidentified species of Caulerpa are new records for the Philippines. Codium cf. latum Suringar (Figure 2) is the only known flattened Codium so far known in the area and the first record of the species for the entire southeast Asia. The list also includes one species new to science, which we describe below.

Figure 2: Codium cf. latum. (2) Habit of pressed specimen of Codium cf. latum, FEUH217, scale = 3 cm. An inset showing its utricle bearing lateral gametangia, scale = 100 µm.

Figure 2:

Codium cf. latum. (2) Habit of pressed specimen of Codium cf. latum, FEUH217, scale = 3 cm. An inset showing its utricle bearing lateral gametangia, scale = 100 µm.

Halimeda magnicuneata Verbruggen et Dumilag, sp. nov. (Figure 3)

Figure 3: Halimeda magnicuneata Verbruggen et Dumilag sp. nov. Holotype specimen of Halimeda magnicuneata, HV823, scale = 1 cm. A diagram showing its cortical utricles, scale = 100 µm.

Figure 3:

Halimeda magnicuneata Verbruggen et Dumilag sp. nov. Holotype specimen of Halimeda magnicuneata, HV823, scale = 1 cm. A diagram showing its cortical utricles, scale = 100 µm.

Holotype: HV823, collected by Heroen Verbruggen in Dancalan, north of Bulusan, SW Luzon, Philippines on 11 February 2004, deposited at BR.

Holotype GenBank accessions: FJ624528 (rbcL), KT887750 (tufA), FJ624604 (ITS nrDNA), FJ624488 (SSU nrDNA), FJ624554 (UCP3) and FJ624834 (UCP7).

Habitat: The type locality is a complex system of crevices shoreward of an exposed coralline reef off Bulusan, Sorsogon, Philippines. The crevices, which are 5–10 m deep and have many vertical walls and overhangs, are sheltered from full wave forces but subject to moderate wave surges. H. magnicuneata was growing on rocky substrate on the vertical walls of the crevices.

Description: Thalli attach to rocky substrata by means of a holdfast disc composed of an intricate network of rhizoidal siphons. The cylindrical to narrow wedge-shaped basal segment is smaller and thicker than the other segments, which are entirely flattened and measure (17-)19–23(-27) mm in length and (15-)17–20(-23) mm in width. The majority of large, flattened segments is ca. 10% longer than wide and is broadest above their middle (at ca. 60–70% from the base). They are wedge-shaped to almost round and lightly calcified.

Medullar siphons are (95-)110–130(-140) µm thick. Subnodal siphons fuse in 2′s or 3′s. The siphons directly above the fusion are (500-)790–1100(-1500) μm long. The cortex consists of two utricle layers, very rarely 3. Peripheral utricles are (39-)42–48(-50) µm in surface diameter and (55-)60–65(-75) µm high. Adjacent peripheral utricles attach to one another at their tips and show an irregular polygonal pattern in surface view, with medium-thickness cell walls and the occasional fusion between adjacent utricles. Secondary utricles are markedly inflated and measure (60-)75–100(115) µm in diameter and (95-)120–160(-185) µm in height. They carry 4–8 peripheral utricles.

Phylogeny: Refer to the phylogenetic analysis of Verbruggen et al. (2009) as inferred from a concatenated alignment of rbcL, tufA, UCP3, UCP7, 18S, and ITS sequences. The node “H. ‘magnicuneata’” refers to the holotype material HV823 from Bulusan, Sorsogon, Philippines.

Distribution:Halimedamagnicuneata confirmed occurrences are so far from Sorsogon, Philippines and Barrow Island, Western Australia.

Table 3 shows the similarities of Ulvophyceae record matrix constructed for each site with Sørensen’s similarity index. The number of species per site varied between 10 and 96 with the highest record from BU, as would be expected considering that the greatest sampling effort was in this site over the past five decades, as compared to the other sites (Figure 4). The ulvophycean flora of eastern Sorsogon represents the highest count with consistently low similarity index as compared to any other region within the Philippines (Table 4).

Table 3:

Pairwise values of Sørensen’s similarity indices based on species composition of Ulvophyceae recorded among the eight sites in eastern Sorsogon.

Site No. of Ulvophyceae species recorded Paired site Sørensen’s similarity index (S)
PD GU BA BU SM MT TI
Prieto Diaz (PD) 18
Gubat (GU) 10 0.30
Barcelona (BA) 30 0.72 0.40
Bulusan (BU) 96 0.89 1.00 0.93
Sta. Magdalena (SM) 50 0.67 0.60 0.60 0.92
Matnog (MT) 16 0.29 0.10 0.53 1.00 0.88
Tikling Is. (TI) 21 0.44 0.20 0.40 1.00 0.82 0.82
Juac Is. (JI) 19 0.39 0.10 0.63 1.00 0.84 0.76 0.79

    S = Ncommon/(Nless), where S represents index of similarity, Ncommon is the number of species held in common between paired sites, and Nless is the total number of species in a site with a lesser species count.

Figure 4: Species accumulation curve of Ulvophyceae taxa recorded for eastern Sorsogon. Study sites with report of Ulvophyceae species for each given year: PD: Prieto Diaz, GU: Gubat, BA: Barcelona, BU: Bulusan, SM: Sta. Magdalena, MT: Matnog, TI: Tikling Is., JI: Juac Is.

Figure 4:

Species accumulation curve of Ulvophyceae taxa recorded for eastern Sorsogon. Study sites with report of Ulvophyceae species for each given year: PD: Prieto Diaz, GU: Gubat, BA: Barcelona, BU: Bulusan, SM: Sta. Magdalena, MT: Matnog, TI: Tikling Is., JI: Juac Is.

Table 4:

Comparison of eastern Sorsogon Ulvophyceae flora among neighbouring areas within the Philippines.

Site References Nb Na+b Cs
Northern Luzon
 Batanes Manza (1939), Cordero (1977) 48 28 0.37
 Ilocos Norte Cordero (1983), Hurtado-Ponce (1983), Marcos-Agngarayngay (1983), Agngarayngay et al. (2005) 56 31 0.39
 Pangasinan Domantay 1961, Trono and Ohno (1992) 46 36 0.48
Southwestern Luzon
 Batangas Villones and Magdamo (1968), Velasquez et al. (1971), Trono and Ohno (1992), Trono and Ganzon Fortes (1980), Roleda et al. (2000) 45 34 0.46
Southeastern Luzon (Bicol Region)
 Albay Mendoza and Soliman (2013), Camaya et al. (2014) 33 22 0.32
 Catanduanes Evangelista et al., 2015 64 43 0.51
Central Philippines
 Cebu Liao and Sotto (1980), Modelo and Umezaki (1987), Belleza and Geraldino (2019) 67 45 0.53
 Panay Cordero (1987), Modelo and Umezaki (1987), Hurtado-Ponce et al. (1992), Luhan et al. (1992), Hurtado-Ponce et al. (1998) 57 43 0.54
 Romblon Clemente et al. (2017) 48 39 0.52
Palawan-Sulu Sea
 Palawan Trono and Ang (1982), Modelo et al. (1989), Santiañez et al. (2015) 78 54 0.60
 Sulu Sea Islands Liao and Young, 2002 33 20 0.29
Western Mindanao
 Sulu (Siasi Is.) Trono (1972b) 42 24 0.33
 Tawi-Tawi Trono (1972c), Puig-Shariff (2015), Dumilag (2019), Tahil and Liao (2019) 48 42 0.56
 Zamboanga del Sur Tito et al. (2000) 36 31 0.45

    Sørensen’s similarity index sensu Magurran (1988): Cs=(2Na + b)/(Na + Nb), where Na is the total number of Ulvophyceae species in eastern Sorsogon (n = 103); Nb is the total species count of the neighbouring site; Na+b is the number of species held in common.

4 Discussion

Our list treats over 50% of the known species of Ulvophyceae reported for the Philippines (as referenced in Ang et al. 2013 with 197 species). Many recent taxonomic changes, often based on molecularly-assisted alpha taxonomic studies, have been incorporated in our present records of Ulvophyceae from eastern Sorsogon. Most ulvophycean taxa that have been reported as new from the area are long known to have wide distributions in many regions in the Philippines (see Silva et al. 1987). Detection of some of these taxa would pass unnoticed by previous surveys, in part due to professional unfamiliarity with species assignment especially those whose key taxonomic characters overlap with other taxa (e.g., Valonia fastigiata Harvey ex J.Agardh as to Valonia utricularis (Roth) C.Agardh, Caulerpa biserrulata Sonder to Caulerpa brachypus Harvey, and Halimeda tuna (J.Ellis et Solander) J.V.Lamouroux to Halimeda gigas W.R.Taylor). Considering their small size, it is possible that Acetabularia dentata Solms-Laubach, Parvocaulis exiguus (Solms-Laubach) S.Berger, Fettweiss, Gleissberg, Liddle, U.Richter, Sawitzky et Zuccarello, and Parvocaulis parvulus (Solms-Laubach) S.Berger, Fettweiss, Gleissberg, Liddle, U.Richter, Sawitzky et Zuccarello have been previously overlooked in the area.

This study has resulted in an increased number of Ulvophyceae species recorded from the Philippines. A. amadelpha, C. buginensis, and one unknown species of Caulerpa are first records for the Philippines.

Avrainvillea amadelpha, originally described from Madagascar, is widely distributed in the tropical Indo-West Pacific, with several records in southeast Asia. Its occurrence in the Philippines is therefore not unexpected. Although identifying A. amadelpha can be difficult (Wade et al. 2018), it can however be distinguished from the morphologically similar species A. lacerata J.Agardh. In the latter species, the stipes are more distinct and the blades composed of tightly woven filaments resulting in a papery texture (Coppejans et al. 2017).

Caulerpa buginensis was described (as C. buginense) from a single specimen from southwest Sulawesi, Indonesia (Verheij and Prud’homme van Reine 1993). It is characterised by two opposite rows of overlapping, compressed, rounded ramuli. This is the second published record of this species and the first outside Indonesia. The specimen from Sorsogon differs from the type specimen by having shorter assimilators with up to six ramuli per rachis side, whereas the type specimen shows up to 21 ramuli pairs.

A sheet lodged at MICH number 679832 (Kraft #340) dated 04 June 1969 is accompanied by a labelled “Caulerpa” handwritten by its collector, G.T. Kraft, with annotations: “like slender (Caulerpa) ashmeadii ramellar (sic ramular) tips rounded; not apiculate” and “more lax and more slender than ashmeadii” (see http://macroalgae.org/portal). Caulerpa ashmeadii is described from Florida and is thought to be restricted to the Atlantic (Pattarach et al. 2019). It belongs to a clade with three other species that are limited to the Atlantic (Sauvage et al. 2014). A few doubtful records exist from the Indo-Pacific, but these have never been confirmed by molecular data (Pattarach et al. 2019). A specimen from Thailand initially identified as C. ashmeadii was molecularly identified as Caulerpa macrodisca (Decaisne) Weber Bosse (Pattarach et al. 2019). Otherwise, the Sorsogon specimen may represent the rare Indo-Pacific species Caulerpa pinnata C.Agardh or Caulerpa lagara Carruthers, Walker et Huisman, which both have terete ramuli without apiculi like C. ashmeadii, but ramuli are sparser than in C. ashmeadii (Carruthers et al. 1993; Greville 1853). Draisma et al. (2014) hypothesised that C. lagara is a synonym of C. pinnata. C. pinnata has been reported from Sri Lanka (type location) and the Red Sea, and C. lagara is known only from its type location in the Swan River, Western Australia, and was never reported since its description. However, currently there is no DNA sequence data available for C. pinnata and C. lagara.

The morphological features of the eastern Sorsogon Codium cf. latum suit the description of Okamura (1915) and Schmidt (1923) for the presence of slightly enlarged utricle apices and gametangia issued from the middle portion of the utricle. Codium latum is an entirely flattened erect species, described from Japan and reported from other regions in the north-western Pacific (Korea and Taiwan) and Indian Ocean, viz. Oman, Yemen, India, and Pakistan (Guiry and Guiry 2020). It constitutes a new record for the southeast Asian waters (i.e., not recorded from any area in this region, see Atmadja and Prud’homme van Reine 2014; Coppejans et al. 2017; Nguyen et al. 2013; Phang et al. 2019; Soe-Htun et al. 2009; Titlyanov et al. 2016); however, it is important to note that genetic analyses have shown that C. latum is not a monophyletic entity (Verbruggen et al. 2007), and the taxonomy of this species across its reported distribution requires revision based on molecular evidence.

The distinction of H. magnicuneata sp. nov. as a separate taxon was supported by previous molecular analyses (Verbruggen et al. 2009). It has been clear for some time that several species of Halimeda are not monophyletic entities (Kooistra et al. 2002; Verbruggen et al. 2005), and in the Indo-Pacific, entities referred to as H. tuna, H. cuneata, and H. discoidea are particularly problematic (Verbruggen et al. 2005). H. magnicuneata shares features with several other species. In its anatomy, it resembles H. discoidea, with inflated secondary utricles bearing many primary utricles, but it differs from that species in having larger segments that are on average more top-heavy (maximum width closer to the top) than those of H. discoidea, although the variability in the latter species is large. The segments are somewhat reminiscent of the wedge-shaped H. cuneata but are wider and generally more rounded. Due to the large and thin segments it also has superficial similarities to H. gigas, but the segments of H. magnicuneata are more top-heavy than those of H. gigas. The inflated secondary utricles of H. magnicuneata make for a clear distinction from both H. cuneata and H. gigas.

The number of ulvophycean species of eastern Sorsogon constitutes the highest, so far, among other regions within the Philippines. The recent comparison, however, might be biased because other areas in the Philippines have been less sampled while those having available regional reports need updating as well. Studies on the red alga Portieria hornemanii (Lyngbye) P.C.Silva (Leliaert et al. 2018; Payo et al. 2013), have indicated that cryptic species diversity can be substantial and that species composition may differ strongly between regions in the Philippines. Intensive sampling in other areas, combined with DNA barcoding, will provide a more realistic view on species diversity in the Philippines.

The increased number of ulvophycean species in the area is consistent with the expectation of a gradual augmentation of species discovery based upon the integration of molecular-assisted taxonomic approaches, particularly in Bulusan, where most of the sampling have been conducted. While DNA barcoding of ulvophycean specimens has greatly improved the discrimination of taxa, an appreciation of the true extent of species richness will certainly remain dependent on the taxonomic expertise of active national and international researchers and the future generations of phycologists that they will be training. It is expected that far greater accuracy will be achieved in the determination of true species richness of the Sorsogon region and, indeed, all Philippine habitats, when rigorous morpho-anatomical, molecular, and ecological studies are thoroughly integrated in the coming years.

Funding source: FEU University Research Center (URC)

Acknowledgments

We are thankful to W.J. E. Santiañez for sorting the Ulvophyceae collection at MSI and to Willem Prud’homme van Reine for useful discussions on Caulerpa. M.Y. Roleda acknowledges the Department of Science and Technology (DOST) Balik Scientist Program for the fellowhip. All Sta. Magdalena and some Bulusan collections deposited at FEU were part of the undergraduate group thesis by F.S. Dumago, R.K.R. Cabudoy, M.C.E. Peralta and C.C. Li.

    Author contribution: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.

    Research funding: This work is partly funded by the FEU University Research Center (URC).

    Conflict of interest statement: The authors declare no conflicts of interest regarding this article.

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Supplementary Material

The online version of this article offers supplementary material (https://doi.org/10.1515/bot-2020-0017).

Received: 2020-03-20
Accepted: 2020-05-27
Published Online: 2020-08-31
Published in Print: 2020-10-25

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