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Philippine Journal of Science 150 (4): 829-844, August 2021 ISSN 0031 - 7683 Date Received: 15 Feb 2021

First Taxonomic Records of Epizoic Freshwater Algae on Golden Apple (Pomacea canaliculata Lamarck) from Rice Paddies in ()

Eldrin DLR. Arguelles*

Philippine National Collection of Microorganisms National Institute of Molecular Biology and Biotechnology (BIOTECH) University of the Philippines Los Baños, College, Laguna 4031 Philippines

In rice paddies where hard substrate is considered as a limiting resource, the hard shell of mollusks can serve as a primary settling space of algal epibionts. The study presents the first taxonomic survey to report and describe epizoic algae in freshwater – golden apple snail (GAS) (Pomacea canaliculata Lamarck) – found in agricultural areas. A total of 17 microalgal taxa belonging to 12 orders, 16 families, and 17 genera were taxonomically identified and described from the collected samples, all of which are considered new distributional records of microalgae in the Philippines. The study shows (six species) as the main group of epizoic microalgae present in shell surfaces of the mollusk, followed by Bacillariophyceae (four species), Chlorophyceae (three species), Zygnematophyceae (two species), Trebouxiophyceae (one species), and Euglenophyceae (one species). Also, the survey reported the occurrence of a photosynthetic euglenoid, Phacus hamatus Pochmann, described for the first time in the Philippines. Diagnostic descriptions and taxonomic keys are presented to differentiate the epizoic algal taxa associated with GAS. The survey shows important taxonomic records on the composition and species diversity of epizoic algae from freshwater snails found in terrestrial habitats of the Philippines.

Keywords: biodiversity, cyanobacteria, microalgae, mollusks, shell,

INTRODUCTION is small and sparse; thus, the ecological importance of this relationship (to such a unique ecosystem) is Microalgae are capable of existing in diverse types of sometimes overlooked. However, recent studies show that benthic substrates. These substrata would include surfaces epizoic algal communities may be useful in ecological of biological (such as mollusks and plants) and non- assessments serving as pollution indicators in an aquatic biological (such as rocks and soil) material (Garbary et al. and terrestrial environment (Ziglar and Anderson 2005). 2007). In rice paddies where hard substrate is considered The relationship of the existence of epizoic algae in shells as a limiting resource, the hard shell of mollusks (such of mollusks is still a poorly understood research topic as GAS) can serve as a primary settling space of algal (Fayolle et al. 2016). Recent studies suggest that the hard epibionts and other invertebrates (Garbary et al. 2007; shell of these animals can act as ecosystem engineers that Fayolle et al. 2016; Damborenea et al. 2017). The can change the species composition and environmental existence of epizoic algae in the hard shell of mollusks characteristics of terrestrial habitats (Abbott and Bergey 2007; Seaborn 2014; Damborenea et al. 2017). In addition, *Corresponding Author: [email protected]

829 Philippine Journal of Science Arguelles: First Taxonomic Records of Epizoic Vol. 150 No. 4, August 2021 Freshwater Algae on Golden Apple Snails the existence of these microalgae in these invertebrates is our local understanding of the algal community existing hypothesized to be symbiotic showing beneficial effects in this peculiar habitat. for each organism. Epizoic algae benefit the host organism by giving an additional food source, mitigating heat stress, and ensuring protection (such as camouflage) with no detrimental effects on the host (Seaborn 2014; Abbott and MATERIALS AND METHODS Bergey 2007). Generally, the shells of freshwater snails are characterized to have scant microalgal growth and few Sampling of Epizoic Algae reported species are documented (Keating and Prezant GAS samples where observable growth of epizoic algae 1998; Damborenea et al. 2017). This is due to factors such was noted were collected from four different rice farming as the production of anti-biofouling chemicals, grazing, sites: Los Baños (situated at 14° 9’ 9.1548” N, 121° 15’ and shell size that have a notable influence on the diversity 30.8772” E), Calauan (situated at 14° 8’ 35.042” N, 121° and distribution of epizoic algae on mollusks (d’Alelio et 18’ 47.2012” E), Magdalena (situated at 14° 12’ 42.1164” al. 2011). On the other hand, there are several factors that N, 121° 25’ 51.798” E), and Bay (situated at 14° 10’ can promote the proliferation of epizoic algae on mollusk 43.0212” N, 121° 17’ 3.5736” E) in Laguna. Epizoic shells such as high nutrient availability in the environment, algae samples were scraped from the shell surfaces of 24 suitable microtopography, and high light intensity (Abbott P. canaliculata, which were collected and attached to the and Bergey 2007; Garbary et al. 2007; d’Alelio et al. 2011; stem and roots of rice in different paddy fields. The algae Fayolle et al. 2016). were gently scraped from the shells using a sterile scalpel. The freshwater mollusk Pomacea canaliculata (Lamarck) The collected samples were divided into two: the first is an invasive species of snail commonly seen in rice group was used to identify the epizoic algae in their living paddies of the Philippines (Basilio 1991). This mollusk state, and the second group was preserved and fixed using is known for its voracious appetite for herbaceous plants 4% formaldehyde for preservation (Arguelles 2020a; and is considered a threat for rice farmers. It is capable Arguelles et al. 2020; Arguelles 2021a). Identification of destroying newly transplanted rice by cutting the basal of cyanobacteria, chlorophytes, charophytes, and portion of young rice seedlings using its (layered euglenophytes was done by characterizing each species ) and utilizing the soft and succulent sheath of the morpho-cytologically both in fresh and preserved samples rice plant. A massive invasion of this mollusk in rice with the aid of available general taxonomic references paddies can cause high damage leading to a significant (Arguelles et al. 2014). From the preserved concentrated loss in rice yield and production (Adalla and Morallo- samples, a portion (3 mL) was used for diatom analysis. Rejesus 1989; Basilio 1991). The GAS is one of the These samples were digested chemically following the most common invertebrates in Philippine rice paddies protocol for diatom cleaning of Round et al. (1990). A and, thus, can provide a good habitat for algal epibionts. portion of the cleaned diatom suspension was dried onto To date, knowledge on epizoic algal diversity in the sterile glass coverslips and mounted. Three slides were Philippines is non-existent since the majority of algal prepared for each sample for microscopic observation taxonomic surveys, biodiversity, and ecological studies and enumeration of microalgae. Diatom slides were focused mainly on aquatic as well as terrestrial habitats also prepared in triplicates for each sample and were (Pantastico 1977; Martinez 1984; Zafaralla 1998; kept in a slide box. The slides were examined using a Arguelles et al. 2014; Arguelles 2016; Martinez-Goss et binocular research microscope (Olympus CX31 with al. 2018; Arguelles 2019a, b, c; Arguelles and Martinez- Infinity X digital camera) and photomicrographs were Goss 2019; Martinez-Goss et al. 2019; Arguelles 2020b; taken (at 1000x magnification). The diatom slides and Arguelles 2021a, b), setting aside small and temporary preserved specimens were kept at the Philippine National benthic biological substrates such as shells of mollusks Collection of Microorganisms (PNCM), National Institute and other aquatic animals. Earlier studies of epizoic of Molecular Biology and Biotechnology (BIOTECH), algae in other countries showed that the diversity of University of the Philippines Los Baños (UPLB), College, algae in this overlooked habitat contain rare and endemic Laguna, Philippines (Arguelles 2021b). species that need further study to elucidate the ecological relationship and significance of these microalgae (Soylu Morphotaxonomic Enumeration and Identification et al. 2006; Abbott and Bergey 2007; Akgül et al. 2014). Morphotaxonomic identification up to the algal species The objective of this study is to provide the first taxonomic level was done making use of all possible and accessible survey of epizoic algae associated with GAS from rice information and literature. The morphological and metric paddies in Laguna, Philippines. This survey will give features important in taxonomic identification such as additional information on the diversity and distribution shape and size of vegetative and specialized (akinetes and of Philippine microalgal flora important for increasing heterocytes) cells, attributes of the cellular protoplasm,

830 Philippine Journal of Science Arguelles: First Taxonomic Records of Epizoic Vol. 150 No. 4, August 2021 Freshwater Algae on Golden Apple Snails

Figure 1. Location map of sampling sites of epizoic algae on Pomacea canaliculata Lamarck from rice paddies in Laguna, Philippines.

number of cells in a colony, characteristics of the by Bacillariophyceae (four species), Chlorophyceae trichomes and filaments such as the presence or absence (three species), Zygnematophyceae (two species), of sheath and constrictions at the cross wall, plus color Trebouxiophyceae (one species), and Euglenophyceae and appearance of the envelopes and sheath were noted (one species). The survey described for the first time during the taxonomic classification and identification of in the Philippines the occurrence of these microalgae each observed epizoic algal taxa. The microalgal taxa in this habitat. Thus, these reported algal taxa are also were identified and described using reference taxonomic considered as new distributional records in the country. literature and monographs done by Desikachary (1959), Taxonomic literature used in the identification, as well as Prescott (1962), Velasquez (1962), Pantastico (1977), comparison of the specimen for each microalgal taxa, are Martinez (1984), Zafaralla (1998), Wehr and Sheath listed directly below the species name. Also, taxonomic (2003), Whitton (2002), John (2002), and Wołowski et comments, distribution, as well as the current accepted al. (2013). taxonomic names based on Algaebase (Guiry and Guiry 2021), are presented in the paper.

RESULTS The taxonomic survey reports a total of 17 epizoic algal species (Table 1) belonging to 12 orders, 16 families, and 17 genera. The study shows Cyanobacteria (six species) as the main group of epizoic microalgae present in shell surfaces of P. canaliculata, followed

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Table 1. Epizoic algae found on Pomacea canaliculata in the study area. Sampling area Taxon Los Baños Calauan Magdalena Bay Cyanobacteria Nostoc commune + Hapalosiphon welwitschii + Gloeotrichia natans + Anabaenopsis circularis + Phormidium breve + + Anabaena sp. + Charophyta Cosmarium sp. + Spirogyra sp. + + Euglenophyta Phacus hamatus* + Bacillariophyta Encyonema perminutum + Halamphora sp. + Navicula sp. + Nitzschia palea + Chlorophyta Chlorella vulgaris + Chlorococcum infusionum + + Kirchneriella lunaris + Coelastrum sp. + *Indicates new record for Philippine algal flora

Dichotomous Key

1. Cells with typical nucleus (eukaryotes); pigments bounded by membranes on specific organelles (chromoplastids) ...... 2 1. Cells without typical nucleus (prokaryotes), chromatinic material irregularly distributed in the central portion of the cell; chromoplastids are absent, pigments dispersed in the peripheral portion of the cell (chromoplasm) ...... 12

2. Cells are motile with red eyespot and proteinaceous pellicle (layer below the plasma membrane that appear as spiral strips) ...... Phacus hamatus 2. Cells without red eyespot and proteinaceous pellicle ...... 3

3. Cells with siliceous cell wall (frustules) and golden brown-colored chloroplasts ...... 9 3. Cells with cell walls made of cellulose and contain green-colored chloroplasts ...... 4

4. Cells are coccoid or filamentous without sexual reproduction by conjugation ...... 6 4. Cells are coccoid or filamentous with sexual reproduction by conjugation ...... 5

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5. Cells are solitary, usually longer than wide, free-living, and capable of semi-cell formation with a median constriction ...... Cosmarium sp. 5. Cells are uniseriate filaments, unbranched and intertwined, and not capable of semi-cell formation ...... Spirogyra sp.

6. Cells are capable of forming coenobia composed of several cells joined by several processes ...... 7 6. Cells are spherical, ovoid, or ellipsoidal occurring as unicellular or in cluster of several cells not capable of forming a coenobium ...... 8

7. Coenobium are spherical made of 8, 16, or 32 cells joined by several processes; cells are ovoid or spherical with a single parietal chloroplast and a pyrenoid ...... Coelastrum sp. 7. Coenobium is made of 2-4-8 up to 64 cluster of crescent-shaped cells sometimes surrounded by a mucilaginous sheath ...... Kirchneriella lunaris

8. Cells are solitary and spherical with a diameter of 9.5–16.0 μm ...... Chlorococcum infusionum 8. Cells are solitary and spherical with a diameter of 1.5–4.0 μm ...... Chlorella vulgaris

9. Valves are semicircular in shape with dorsal margin that is distinctly curved, while the ventral margin is straight ...... Encyonema perminutum 9. Valves are lanceolate, linear-lanceolate, semi-lanceolate, or elliptical rounded in shape ... 10

10. Valves are linear-lanceolate in shape with narrowly elongated capitate ends ...... Nitzschia palea 10. Valves are semi-lanceolate or elliptical rounded in shape ...... 11

11. Valves linear-lanceolate with convex dorsal margin and straight, linear ventral margin; apices ventrally curved and capitate ...... Halamphora sp. 11. Valves are elliptical rounded in shape and with a raphe that is filiform and straight ...... Navicula sp.

12. Trichomes are uniseriate and irregularly arcuate exhibiting “true branching,” slightly Hapalosiphon constricted at the cross walls; apices are capitated and not attenuated ...... welwitzschii 12. Trichomes may exist as straight or circular and spirally-coiled not capable of exhibiting “true branching” with or without mucilaginous sheath; filaments may or may not be attenuated ...... 13

13. Trichomes are uniseriate and straight having filaments not capable of forming specialized cells (akinetes and heterocytes) ...... Phormidium breve 13. Trichomes are uniseriate, straight, circular, or spirally-coiled and with filaments that have specialized cells (akinetes and heterocytes) ...... 14

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14. Trichomes are circular and spirally-coiled with constrictions at the cross walls; filaments with cells that are barrel-shaped or cylindrical ...... Anabaenopsis circularis 14. Trichomes are straight, uniseriate with constricted cross walls; filaments have cells that are ellipsoidal, spherical, or short barrel-shaped ...... 15

15. Trichomes are broad, slightly bent, or curved, usually ending in a distinct hair with filaments that have spherical basal heterocytes ...... Gloeotrichia natans 15. Trichomes are straight and uniseriate with filaments that have constricted cross walls and specialized cells (heterocytes and akinete) that are intercalary ...... 16

16. Trichomes are uniseriate, enveloped within a gelatinous sheath, and with filaments that have constricted cross walls ...... Nostoc commune 16. Trichomes are solitary, straight, isopolar, uniseriate not enveloped within a gelatinous sheath, and with filaments that have constricted cross walls ...... Anabaena sp.

Phylum: CYANOBACTERIA Genus: Hapalosiphon Nägeli ex É. Bornet & C. Flahault Class Cyanophyceae Order: 1. Hapalosiphon welwitschii West & G.S. West Family: Nostocaceae Pl. I, Fig. 2 Genus: Nostoc Nägeli References: Desikachary (1959), Cyanophyta, 588p., Pl. 1. Nostoc commune Vaucher ex Bornet & Flahault 137, Fig. 5; Martinez (1984), A Checklist of Blue-Green Pl. I, Fig. 1 Algae of the Philippines, 39p.; Arguelles and Monsalud (2017), Phil J System Biol, 32p., Pl. I, Fig. 7. References: Desikachary (1959), Cyanophyta, 387p., Pl. 68, Fig. 3.; Martinez (1984), A Checklist of Blue-Green Trichomes are uniseriate and unevenly arcuate showing Algae of the Philippines, 52p.; Arguelles and Monsalud “true branching,” slightly constricted at the cross walls, (2017), Phil J System Biol, 32p., Pl. I, Fig. 8. and apices are capitated and not attenuated. Cells are cylindrical, blue-green in color, 3.0–5.0 µm long and Trichomes are uniseriate usually enveloped within a 2.0–4.0 µm wide, protoplasm not granular, and sheaths are gelatinous sheath. Cells are bluish-green in color, nearly colorless and thin. Lateral branches are short, with almost spherical or short barrel-shaped, 3.5–6.0 μm in length, and similar measurements as the main filament. 2.5–4.0 μm in width. Heterocytes are broadly ellipsoidal or sub-spherical, 5.0–6.0 μm in length, and 4.0–5.0 μm in Specimen: , Laguna, Los Baños (UPLB Center width. Akinetes are rarely observed, 3.6–6.3 μm in length, for Technology Transfer and Entrepreneurship, Biotech and 3.5-4.0 μm in width. Road, rice paddies), E.DLR. Arguelles s.n. (Herb. No. AC12-1-a-c, PNCM). Specimen: Luzon, Laguna, Magdalena (Brgy. Salasad, rice paddies), E.DLR. Arguelles s.n. (Herb. No. AC11- Distribution in the Philippines: Laguna, Los Baños, 1-a-c, PNCM). Mayondon (on flowing water, creek, the shoreline of ; Pantastico 1977); Laguna, Los Banos Distribution in the Philippines: Palawan, Araceli, (on [Philippine Rice Research Institute (PhilRice) substation grasses as yellowish-brown to black growth; Velasquez (paddy fields); Arguelles and Monsalud 2017]; Laguna, 1962); Nueva Vizcaya, Bayombong (rice paddies) Los Baños (this specimen is a new distributional record). Pantastico and Gonzales (1976); Laguna, Los Baños (rice paddies) Arguelles and Monsalud (2017); Laguna, Class Cyanophyceae Magdalena (this specimen is a new distributional record). Order: Nostocales Family: Gloeotrichiaceae Class Cyanophyceae Genus: Gloeotrichia J. Agardh ex Bornet & Flahault Order: Nostocales Family: Hapalosiphonaceae

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1. Gloeotrichia natans Rabenhorst ex Bornet & Distribution in the Philippines: Laguna, Los Baños (Tadlak Flahault Pl. I, Fig. 3 Lake; Gonzales 1961); Laguna, Los Baños, (Laguna de Bay; Velasquez (1962); , Navotas, Malabon References: Martinez (1984), A Checklist of Blue-Green (fishponds, stomach of milkfish Chanos chanos Forsk.; Algae of the Philippines, 38; Deep et al. (2013), Aquat Vicencio 1977); Camarines Sur, Sta. Cruz, (sanctuary, Biosys, 6p., Fig. 3.19. inlets of Lake Buhi; Baloloy et al. 2016); Laguna, Filaments are loosely arranged. Trichomes are 7.0–8.0 μm, Magdalena (this specimen is a new distributional record). broad, slightly bent/curved, and usually ending in a distinct Class Cyanophyceae hair. Cells at the base are barrel-shaped, as long as broad Order: Nostocales or sometimes shorter. Heterocytes are basal, more or less Family: Aphanizomenonaceae spherical, and 5.0–12.0 μm broad. Akinetes are cylindrical, Genus: Anabaenopsis (V.V. Miller) straight, or curved with a sheath 12.0–20.0 μm broad and 35.0–67.0 μm, without sheath up to 35.0 μm broad, saccate, 1. Anabaenopsis circularis (G.S. West) Woloszynska hyaline, or brownish with the smooth cell wall. & V. Miller Pl. I, Fig. 5 Specimen: Luzon, Laguna, Calauan (Brgy. Kanluran, rice Basionym: Anabaena flosaquae var. circularis G.S. West paddies), E.DLR. Arguelles s.n. (Herb. No. AC13-1-a-c, PNCM). References: Martinez (1984), A Checklist of Blue-Green Algae of the Philippines, 24; Arguelles (2019a), Pertanika Distribution in the Philippines: Laguna, Los Baños, J Trop Agric Sci, 826p., Fig. 3e. Mayondon (on the shoreline of Laguna de Bay; Pantastico (1977); Laguna, Los Baños, IRRI ricefield (epiphytic on Trichomes are constricted at the cross walls without aquatic weeds; Kulasooriya et al. (1981); Laguna, Calauan mucilaginous sheath, circular, and spirally-coiled. Cells (this specimen is a new distributional record). are barrel-shaped or cylindrical, 7.0–10.0 μm long, 2.5–4.5 μm wide, and slightly curved with aerotopes. Specialized Class Cyanophyceae cells like heterocytes are usually in the apical end, ovoid, Order: Nostocales or spherical in shape and 3.0–4.0 μm in diameter. On Family: Nostocaceae the other hand, akinetes are solitary, oval, or elliptical, Genus: Anabaena Bory ex Bornet & Flahault 7.5–10.5 μm long, and 5.5–6.0 μm wide. 1. Anabaena sp. Pl. I, Fig. 4 Specimen: Luzon, Laguna, Los Baños (UPLB Center for Technology Transfer and Entrepreneurship, Biotech References: Komárek and Johansen (2015), Filamentous Road, rice paddies), E.DLR. Arguelles s.n. (Herb. No. Cyanobacteria. In Freshwater Algae of North America: AC12-1-a-c, PNCM). Ecology and Classification, 216p., Fig. 42. Distribution in the Philippines: Laguna, Los Baños (Tadlak Trichomes are solitary, isopolar, and uniseriate with Lake; Gonzales 1961); Laguna, Victoria (submerged stem filaments that have constricted cross walls. Cells are and roots of water spinach; Arguelles 2019a); Laguna, ellipsoidal, spherical, cylindrical, pale to blue-green in Los Baños (this specimen is a new distributional record). color with granular contents and without aerotopes, 6.5– 8.0 μm in length, and 5.0–6.5 μm in width. Heterocytes Class Cyanophyceae are solitary and intercalary, 7.0–9.5 μm in length, and Order: Oscillatoriales 5.5–7.0 μm in width. Akinetes are solitary, cylindrical, Family: Oscillatoriaceae and intercalary, 7.5–10.5 μm in length, and 6.0-7.7 Genus: Phormidium Kützing ex Gomont μm in width. The specimen showed characteristics of the vegetative and specialized cells. Details of the 1. Phormidium breve (Kützing ex Gomont) Anagnostidis mucilaginous sheath, trichome features (straight form, & Komárek Pl. I, Fig. 6 regularly coiled, circinate, or irregularly coiled) – as Basionym: Oscillatoria brevis Kützing ex Gomont well as the frequency of akinete and heterocytes (number per filaments and sheath), which are critical in species References: Velasquez (1962), Philipp J Sci 91(3): 296, identification of the alga – were not observed or visible Pl. 2, Fig. 31; Martinez (1984), A Checklist of Blue-Green in the prepared specimens. Algae of the Philippines, 57p.; Gaysina et al. (2018), Cryptogam Algol, 18p., Fig. 32. Specimen: Luzon, Laguna, Magdalena (Brgy. Salasad, rice paddies), E.DLR. Arguelles s.n. (Herb. No. AC11- Trichomes are dark blue-green in color without 1-a-c, PNCM). constrictions at the cross walls. Filaments are slightly curved or straight with attenuated ends (hooked and bent).

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Plate I. Photomicrographs of 1) Nostoc commune Vaucher ex Bornet & Flahault, 2) Hapalosiphon welwitschii West & G.S. West, 3) Gloeotrichia natans Rabenhorst ex Bornet & Flahault, 4) Anabaena sp., 5) Anabaenopsis circularis (G.S. West) Woloszynska & V. Miller, 6) Phormidium breve (Kützing ex Gomont) Anagnostidis & Komárek, 7) Cosmarium sp., 8) Spirogyra sp., 9) Phacus hamatus Pochmann. All scale bars = 10 μm unless specified otherwise.

Cells are 1.5–2.5 μm in length and 0.4–1.2 μm in width. Phylum: CHAROPHYTA Apical end cells are usually rounded and sometimes Class: Zygnematophyceae obtuse-conical and without calyptra. Order: Desmidiales Family: Desmidiaceae Specimen: Luzon, Laguna, Bay (Brgy. Dila, rice paddies) Genus: Cosmarium Corda ex Ralfs and Calauan (Brgy. Kanluran, rice paddies), E.DLR. Arguelles s.n. (Herb. No. AC14-1-a-c, PNCM). 1. Cosmarium sp. Pl. I, Fig. 7 Distribution in the Philippines: Sulu, Bongao, Tawi- Reference: Gerrath (2003), Conjugating Green Algae and Tawi (polluted pond; Velasquez 1955); Palawan, Puerto Desmids. In Freshwater Algae of North America: Ecology Princesa, Araceli (on muddy substratum; Velasquez and Classification, 374p. Figs. 22–26, 32, and 71–75. 1962); Laguna, Bay and Calauan (this specimen is a new distributional record). Cells are solitary, usually longer than wide, free-living, and with a median constriction, 138.0–227.0 μm in length, and 77.0–122.0 μm in width. Semicells are pyramidal in

836 Philippine Journal of Science Arguelles: First Taxonomic Records of Epizoic Vol. 150 No. 4, August 2021 Freshwater Algae on Golden Apple Snails outline, convex lateral margins, smooth cell wall, and Order: Euglenida rounded apical ends; chloroplasts for each semi-cell Family: Phacidae contain a single pyrenoid. The specimen only shows the Genus: Phacus Dujardin shape, size, and outline of the cells with few characteristics of the chloroplasts. Details of the cell wall ornamentations 1. Phacus hamatus Pochmann Pl. I, Fig. 9 – as well as characteristics and configuration of the References: Wolowski (1998), Frag Flor Geobot Suppl, chloroplasts, which are critical in species identification 78p., Figs. 265–266; Alves-da-Silva and Bicudo (2009), of the alga – are not visible in the prepared specimen. Revista Brasil Bot, 261 p., Figs. 39–43. Specimen: Luzon, Laguna, Bay (Brgy. Dila, rice paddies), Cells are broadly oval to round with a red eyespot and E.DLR. Arguelles s.n. (Herb. No. AC14-1-a-c, PNCM). paramylon body at the central part of the protoplasm. Distribution in the Philippines: Camarines Sur, Sta. Cruz, The cellular dimension of the alga is 46.5–48.0 μm long (sanctuary, inlets of Lake Buhi; Baloloy et al. 2016); and 29.0–30.5 μm wide. Several discoid chloroplasts are Laguna, Calauan, (phytotelmata of pineapple; Arguelles present within the cytoplasm. Longitudinally striated 2020a); Laguna, Bay (this specimen is a new distributional pellicles are present, covering the cell. The flagellum is record). shorter than the total cell length. The posterior end of the cell is characterized by a slightly curved cauda. Class: Zygnematophyceae Order: Zygnematales Specimen: Luzon, Laguna, Los Baños (UPLB Center Family: Zygnemataceae for Technology Transfer and Entrepreneurship, Biotech Road, rice paddies), E.DLR. Arguelles s.n. (Herb. No. Genus: Spirogyra Link AC12-1-a-c, PNCM). 1. Spirogyra sp. Pl. I, Fig. 8 Distribution in the Philippines: a new record for the References: Hall and McCourt (2015), Conjugating Green Philippines Algae Including Desmids, In: Freshwater Algae of North America. Ecology and Classification, 442p., Fig. 1, 6–7. Phylum: BACILLARIOPHYTA Class: Bacillariophyceae The thallus is composed of uniseriate filaments, Order: Cymbellales unbranched, and intertwined. Cells are uninucleated and Family: Gomphonemataceae cylindrical (40.0–45.0 µm in width and 161.0–185.0 µm Genus: Encyonema Kützing in length). Parietal chloroplasts are ribbon-like, coiled, and spirally arranged in the cell membrane. Chloroplasts 1. Encyonema perminutum Krammer Pl. II, Fig. 1 are usually 1–15 per cell containing several disc-shaped Reference: Bahls et al. (2018), PhytoKeys, 159p., Pl. pyrenoids. The specimen only shows the shape, size, 122, Figs. 12–13. and characteristics of the algal cells and filaments with a visible configuration of the chloroplasts. Details of Valves are semicircular, 23.9–32.5 μm in length, and the reproductive structure (such as zygospores and 6.50–7.50 μm in width; dorsal margin is distinctly curved conjugating filaments), which is critical in species while the ventral margin is linear and straight; raphe ends identification of the alga, are not visible in the prepared are usually deflected ventrally; striae is 10–13 rows in specimen. 10 μm. Specimen: Luzon, Laguna, Los Baños (UPLB Center Specimen: Luzon, Laguna, Magdalena (Brgy. Salasad, for Technology Transfer and Entrepreneurship, Biotech rice paddies), E.DLR. Arguelles s.n. (Herb. No. AC11- Road, rice paddies) and Calauan (Brgy. Kanluran, rice 1-a-c, PNCM). paddies), E.DLR. Arguelles s.n. (Herb. No. AC13-1-a-c, Distribution in the Philippines: Laguna, (Caliraya PNCM). Lake; Martinez-Goss et al. 2013); Laguna, Magdalena Distribution in the Philippines: Laguna, Los Baños, (this specimen is a new distributional record). Mayondon (on shoreline of Laguna de Bay; Pantastico Class: Bacillariophyceae 1977); , Taal (Taal Lake; Zafaralla 1998); Order: Thalassiophysales Laguna, San Pablo (Sampaloc Lake; de Asis and Zubiaga Family: Catenulaceae 2011); Laguna, Calauan and Los Baños (this specimen is Genus: Halamphora (Cleve) Mereschkowsky a new distributional record). 1. Halamphora sp. Pl. II, Fig. 2 Phylum: EUGLENOPHYTA Class: Euglenophyceae

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Reference: Kociolek et al. (2015), Bacillariophyceae: The Class: Bacillariophyceae Raphid Diatoms. In Freshwater Algae of North America: Order: Bacillariales Ecology and Classification, 751p., Figs. 15M–O. Family: Bacillariaceae Genus: Nitzschia Hassall Valves are dorsiventral, semi-lanceolate, with convex dorsal margin, and straight, linear ventral margin. The 1. Nitzschia palea (Kützing) W. Smith Pl. II, Fig. 4 dorsal margin is longer than the ventral margin. Apices are curved ventrally and capitate with a straight, narrow Basionym: Synedra palea Kützing axial area. Dorsal striae are punctuate and radiate, while Reference: Akbulut (2003), Turk J Bot, 293p., Fig. 5.17; ventral striae are inconspicuous. The dimension of the Arguelles (2020b), Walailak J Sci & Tech, 253p., Pl. III, valves is 22.5–26.7 µm in length and 5.5–6.9 µm in width. Fig. 3. The specimen showed the shape, symmetry, and size of the valves as well as the characteristics of the striae Valves are linear-lanceolate with narrowly elongated capitate of the diatom. Details of the dorsal and ventral fascia, ends. Fibulae are distinct and equidistant (9–15 rows in 10 arrangement of areolae (in the striae), and characteristics μm) with slightly visible and moderately dense striae. Valves of raphe (in the valve surface) – which are critical in are 23.0–31.0 μm in length and 4.0–4.5 μm in width. species identification of the diatom – are not visible in Specimen: Luzon, Laguna, Los Baños (UPLB Center the prepared specimen. for Technology Transfer and Entrepreneurship, Biotech Specimen: Luzon, Laguna, Magdalena (Brgy. Salasad, Road, rice paddies), E.DLR. Arguelles s.n. (Herb. No. rice paddies), E.DLR. Arguelles s.n. (Herb. No. AC11- AC12-1-a-c, PNCM). 1-a-c, PNCM). Distribution in the Philippines: Laguna, Los Baños, Distribution in the Philippines: Palawan, Coron (Maquinit Mayondon (on shoreline of Laguna de Bay; Pantastico Hot Springs; Martinez-Goss et al. 2019); Laguna, 1977); Laguna, Lumban (Caliraya Lake; Martinez-Goss Magdalena (this specimen is a new distributional record). et al. 2013); Laguna, Los Baños, Bayan (submerged roots and stems of pink lotus; Arguelles 2020b); Laguna, Los Class: Bacillariophyceae Baños (this specimen is a new distributional record). Order: Naviculales Family: Naviculaceae Phylum: CHLOROPHYTA Genus: Navicula Bory Class: Trebouxiophyceae Order: Chlorellales 1. Navicula sp. Pl. II, Fig. 3 Family: Chlorellaceae Reference: Kociolek et al. (2015), Bacillariophyceae: The Genus: Chlorella Beyerinck [Beijerinck] Raphid Diatoms. In Freshwater Algae of North America: 1. Chlorella vulgaris Beyerinck [Beijerinck] Ecology and Classification, 745p., Figs. 9A–E. Pl. II, Fig. 5 Valves are elliptical, rounded, or broadly lanceolate References: Prescott (1962), Algae of the Western Great (34.5–36.5 µm in length and 6.0-–7.5 µm in width). Lakes Area, 237, Pl. 53, Fig. 13; Arguelles and Monsalud The raphe is filiform and straight with striations that are (2017), Philipp J System Biol, 31p., Pl. II, Fig. 4; Arguelles highly variable. Striae are 5.0–7.0 rows in 10 μm. The (2019a), Pertanika J Trop Agric Sci, 819p., Fig. 1a; specimen showed the shape, symmetry, and size of the Arguelles (2021b), Phil J Sci, 129p., Pl. I, Fig. 1. valves as well as some observable features of the raphe of the diatom. Details of the arrangement of areolae (in Cells are spherical or ellipsoidal (1.5–4.0 μm in diameter), the striae) and features of the proximal and terminal raphe solitary, and with a very thin and smooth cell wall. end (characteristics of fissures at the raphe ends), which Chloroplast is parietal, cup-shaped, and solitary with a are critical in species identification of the diatom, are not single pyrenoid found at the basal portion of the cell. visible in the prepared specimen. Specimen: Luzon, Laguna, Bay (Brgy. Dila, rice paddies), Specimen: Luzon, Laguna, Bay (Brgy. Dila, rice paddies), E.DLR. Arguelles s.n. (Herb. No. AC14-1-a-c, PNCM). E.DLR. Arguelles s.n. (Herb. No. AC14-1-a-c, PNCM). Distribution in the Philippines: Laguna, Los Baños, Distribution in the Philippines: Laguna, Los Baños, Mayondon (on shoreline of Laguna de Bay; Pantastico Mayondon (on the shoreline of Laguna de Bay; Pantastico 1977); Laguna, Los Baños, (rice paddies; Arguelles and 1977); Laguna, Lumban (Caliraya Lake; Martinez- Monsalud 2017); Laguna, Los Baños, Tadlak (submerged Goss et al. 2013); Laguna, Bay (this specimen is a new roots and stems of water spinach; Arguelles 2019a); distributional record). Laguna, San Antoñio (phytotelmata of Neoregelia

838 Philippine Journal of Science Arguelles: First Taxonomic Records of Epizoic Vol. 150 No. 4, August 2021 Freshwater Algae on Golden Apple Snails

Plate II. Photomicrographs of 1) Encyonema perminutum Krammer, 2) Halamphora sp., 3) Navicula sp., 4) Nitzschia palea (Kützing) W. Smith, 5) Chlorella vulgaris Beyerinck [Beijerinck], 6) Chlorococcum infusionum (Schrank) Meneghini, 7) Kirchneriella lunaris (Kirchner) Möbius, and 8) Coelastrum sp. All scale bars = 10 μm unless specified otherwise.

cruenta; Arguelles 2021b); Laguna, Bay (this specimen System Biol, 30p., Pl. I Fig. 9. is a new distributional record). The microalga is unicellular, green, and occurring either Class: Chlorophyceae as solitary cells or in colonial form (cluster of cells). Cells Order: Chlamydomonodales vary in size usually 9.5–16.0 μm in diameter. Young cells Family: Chlorococcaceae are spherical and have a thin cell wall while mature cells Genus: Chlorococcum Meneghini have irregular outlines with a thick cell wall. Chloroplasts are nearly filling the cell with a single pyrenoid. 1. Chlorococcum infusionum (Schrank) Meneghini Pl. II, Fig. 6 Specimen: Luzon, Laguna, Calauan (Brgy. Kanluran, rice paddies) and Magdalena (Brgy. Salasad, rice paddies), Basionym: Lepra infusionum Schrank E.DLR. Arguelles s.n. (Herb. No. AC13-1-a-c, PNCM). References: Pantastico (1977), Taxonomy of the Distribution in the Philippines: Laguna, Mayondon (on Freshwater Algae of Laguna de Bay and Vicinity, 76p., shoreline of Laguna de Bay; Pantastico 1977); Batangas, Pl. VII, Fig. 1; Zafaralla (1998), Microalgae of Taal Lake, Taal (Taal Lake; Zafaralla 1998); Laguna, Los Baños (rice 33p., Pl 8e.f.; Arguelles and Monsalud (2017), Philipp J

839 Philippine Journal of Science Arguelles: First Taxonomic Records of Epizoic Vol. 150 No. 4, August 2021 Freshwater Algae on Golden Apple Snails paddies; Arguelles and Monsalud 2017); Laguna, Calauan, Specimen: Luzon, Laguna, Los Baños (UPLB Center Masiit (phytotelmata of Neoregelia compacta; Arguelles for Technology Transfer and Entrepreneurship, Biotech 2021b); Laguna, Calauan and Magdalena (this specimen Road, rice paddies), E.DLR. Arguelles s.n. (Herb. No. is a new distributional record). AC12-1-a-c, PNCM). Class: Chlorophyceae Distribution in the Philippines: Batangas, Taal (Taal Lake; Order: Sphaeropleales Zafaralla 1998); Laguna, Calauan, Masiit (phytotelmata Family: Selenastraceae of Neoregelia compacta; Arguelles 2021b); Laguna, Los Genus: Kirchneriella Schmidle Baños (this specimen is a new distributional record). 1. Kirchneriella lunaris (Kirchner) Möbius Pl. II, Fig. 7 Basionym: Rhapidium convolatum var. lunare Kirchner DISCUSSION Reference: Arguelles (2020a), Phil J Sci, 594p., Pl. I, The study is the first taxonomic survey in the Philippines Fig. 1. to focus on the diversity of epizoic algae of GAS (Pomacea canaliculata) from rice paddies found in Cells are uninucleated, flat, curved, and crescent-shaped Laguna. A total of 17 microalgal taxa were identified with a smooth cell wall. The colony is composed of 2-4- and described from the collected shell samples (Table 1), 8 up to 64 clusters of cells sometimes surrounded by a all of which are considered new distributional records of mucilaginous sheath with a cellular dimension of 2.0–6.5 microalgae in the Philippines (Velasquez 1962; Martinez x 2.7–3.5 µm (length x width). Parietal chloroplasts are 1984; Pantastico 1977; Zafaralla 1998; Arguelles 2016; present with 1–3 pyrenoids (per cell). Martinez-Goss et al. 2018; Arguelles 2019d; Arguelles and Martinez-Goss 2019; Arguelles 2021a, b). Also, the survey Specimen: Luzon, Laguna, Calauan (Brgy. Kanluran, rice reported the occurrence of a photosynthetic euglenoid, paddies), E.DLR. Arguelles s.n. (Herb. No. AC13-1-a-c, Phacus hamatus Pochmann, described for the first time PNCM). in the Philippines. The results show that shell surfaces Distribution in the Philippines: Batangas, Taal (Taal Lake; of freshwater mollusks such as P. canaliculata can serve Zafaralla 1998). Laguna, Calauan, Masiit (phytotelmata as a suitable habitat for the existence of algal epibionts. of Ananas comosus; Arguelles 2020a); Laguna, Calauan During the sampling period, GAS was very abundant in (this specimen is a new distributional record). rice paddies. Hence, it would play a significant biological Class: Chlorophyceae interaction with other microorganisms in the terrestrial Order: Sphaeropleales habitat. The mollusk shells are biogenic in nature and reports Family: Scenedesmaceae regarding bioactive chemicals with anti-fouling activity are Genus: Coelastrum Nägeli few, being restricted only to inhibitory activities against marine species of and (Bers et al. 2006; 1. Coelastrum sp. Pl. II, Fig. 8 Abbott and Bergey 2007). And to date, chemical anti-fouling Reference: Shubert and Gärtner (2015), Non-motile activities of shells from gastropods have not been reported Coccoid and Colonial Green Algae, In: Freshwater Algae (Abbott and Bergey 2007). Generally, snails provide substrata of North America: Ecology and Classification, 336p. Figs. for algal growth and, in turn, the epizoic algae provide extra 7C, D, and 8E. food resources in its host, as well as other epibionts present in the shell surface (Abbott and Bergey 2007). Cells are globose or ovoid with a smooth cell wall and parietal chloroplasts with a cellular dimension of 10.0– Comparison of the species richness epizoic algae observed 13.0 µm in diameter. Coenobium is composed of 2-4-8 up in this study with those observed from freshwater snails to 32 cells with a diameter of 33.0–62.0 µm in diameter. and turtles from previous studies indicated Kirchneriella The specimen showed the shape and size of the algal cells lunaris, Nitzschia palea, Coelastrum sp., Spirogyra sp., as well as the number of cells per coenobium. Details of and Navicula sp. as algal taxa in common (Soylu et al. the characteristics of the interconnecting processes and 2006; Abbott and Bergey 2007). In terms of microalgal gelatinous sheath (surrounding each cell) – as well as diversity, this study showed greater species diversity the features and configuration of the chloroplasts, which as compared to the taxonomic study of epizoic algae are critical in species identification of the alga – are not from freshwater turtles done by Akgül et al. (2014) and observable in the prepared specimen. Garbary et al. (2007), where they reported not more than 14 microalgal taxa from their survey (Table 1). In these studies, microalgal taxa belonging to Chlorophyta

840 Philippine Journal of Science Arguelles: First Taxonomic Records of Epizoic Vol. 150 No. 4, August 2021 Freshwater Algae on Golden Apple Snails and Cyanobacteria are the dominant group of epizoic agricultural areas. Epizoic algae have been reported in algae in shell surfaces of turtles, and no diatom species seawater snails such as those survey done by d’Alelio et al. were documented. The result of these taxonomic (2011), wherein epizoic diatoms attached to seven marine surveys is contrary to those found in the current study snails (Alvania lineata, Bittium reticulatum, Clanculus where cyanobacteria, diatoms, and green algae are the cruciatus, Columbella rustica, Gibbula adansoni, dominant species in shell surfaces of P. canaliculata. This Nassarius incrassatus, and Jujubinus striatus) were observation is similar to that observed by di Persia and described, as well as those done by Muciño-Marquez et Radici de Cura (1973) regarding the diversity of epizoic al. (2021), wherein epizoic algae were reported in Lobatus algae associated with three native species of Pomacea gigas larvae. Generally, there are only few taxonomic (P. canaliculata, P. maculate, and P. scalaris) frequently surveys showing the diversity of epizoic algae in animals inhabiting the River Basin of Río de la Plata in Brazil, found in both terrestrial and aquatic environments. Thus, wherein taxa of epizoic algae (such as Oedogonium additional diversity and ecological studies are needed sp., Stigeoclonium sp., Gomphonema sp., and other to assess and further expand our knowledge on the Oscillatoriales species) together with other groups significance of the symbiotic relationship of these algal of epibionts (nematodes, ciliates, flatworms, rotifers, epibionts on their host organisms. Also, an ecological bryozoans, dipterans, and oligochaetes) were documented assessment of the effect of different factors such as in the survey. Likewise, the dominance of cyanobacteria physical stress, predation, fouling, competition, and and diatoms in shell surfaces of P. caniculata (this study) recruitment dynamics is recommended in taxonomic were also observed by Muciño-Marquez et al. (2021) studies to further elucidate the pattern of distribution, from epizoic algae of gastropod mollusk, Lobatus gigas. succession, and algal species composition within epibiotic The genera Chlorococcum, Spirogyra, and Phormidium communities existing in this unique habitat. were the most frequent and dominant (in terms of algal density) algal species in the collected shell samples of P. canaliculata. In addition, some microalgal taxa such as Phacus hamatus and Coelastrum sp. are found CONCLUSION exclusively in shell surfaces of P. canaliculata collected The current investigation is the first taxonomic survey from Los Baños, Laguna. Several species of euglenoids to report and describe epizoic algae in freshwater snails such as Colacium, Euglena, Phacus, Strombomonas, found in agricultural areas. In addition, it is the first and Trachelomonas, are able to produce polysaccharide taxonomic account in the Philippines to focus on the (Linton et al. 2010). This substance enables these species composition of epizoic algal community existing euglenoids to be attached to living (e.g. zooplankton, in shell surfaces of Pomacea canaliculata (Lamarck) filamentous and planktonic algae), as well as non-living from different rice paddies in Laguna. The survey reports solid substrates (e.g. rock, soil, and shells of animals) a total of 17 epizoic algal species as new distributional (Linton et al. 2010; Karnkowska et al. 2015). In addition, records of microalgae in the Philippines. Also, the the presence of the muciferous bodies under the pellicle occurrence of a microalga, Phacus hamatus Pochmann, of these euglenoid species enables these organisms to is described for the first time in the Philippines. This form extracellular muciferous stalks, loricae, and cysts study highlighted the importance of terrestrial mollusks (Karnkowska et al. 2015; Zakryś et al. 2017). These as a peculiar habitat for the existence of diverse and reported structures and substances are important for the rare species of microalgae. The current investigation is survival of euglenoids in aquatic and terrestrial habitats considered a preliminary taxonomic study on the species and support the existence of Phacus hamatus in shell composition and diversity of epizoic algae found in the surfaces of P. canaliculata observed in this study. Several shell surface of P. canaliculata since limited samples were euglenoid species were also documented in different analyzed in the survey. It is important to take note that a taxonomic surveys such as those done by Fayolle et al. sufficient number of shell samples is needed to be able (2016) and Soylu et al. (2006) on shell surfaces of pond to establish the overall species richness and diversity of turtles (Emys orbicularis), where they reported species epizoic algae associated with P. canaliculata. Thus, the of Euglena acus, E. tripteris, E. contabrica, E. viridis, author recommends in future studies the establishment of Phacus orbicularis, Trachelomonas hispida, and T. nigra a rarefaction curve that will allow the proper calculation as epizoic algal species found in this animal. Thus, epizoic of species richness of epizoic algae for a given number freshwater microalgal taxa that were observed in each of P. canaliculata shell samples. sampling site would contain unique and specific algal species with high tolerance to different habitat conditions. The current study is the first taxonomic survey to report and describe epizoic algae in freshwater snails found in

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