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First Taxonomic Records of Epizoic Freshwater Algae on Golden Apple Snails (Pomacea Canaliculata Lamarck) from Rice Paddies in Laguna (Philippines)

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First Taxonomic Records of Epizoic Freshwater Algae on Golden Apple Snails (Pomacea Canaliculata Lamarck) from Rice Paddies in Laguna (Philippines) 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 Snails (Pomacea canaliculata Lamarck) from Rice Paddies in Laguna (Philippines) 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 snail – 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 Cyanobacteria (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, taxonomy 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 radula (layered euglenophytes was done by characterizing each species tooth) 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
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