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Smithsonian National Museum of Natural History
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Ceratocorys horrida

Introduction

Dr. Maria Faust, a Dinoflagellate Phycologist in the Department of Botany, National Museum of Natural History, is using the Scanning Electron Microscope (SEM), for identifying the biodiversity of dinoflagellates in The Gulf Stream off the Indian River Inlet Florida, and The Atlantic Barrier Coral Reef -Mangrove Ecosystems Belize, Central America. It is a little-known fact that only a small percentage of the living dinoflagellate algae of the species-rich marine ecosystem is known or illustrated. Results suggest that they are an important microscopic component of the marine food web. They are able to exploit the environment to their benefit in order to survive and proliferate. The primary tasks of collection related research have been documenting how ecological, physiological, and environmental interactions may affect species diversity and the distribution of toxic and nontoxic dinoflagellates. This very old and successful group of unicellular aquatic, eukaryotic microorganisms comprises a large number of algal species of many shapes and sizes. Examples of species are illustrated in the attached SEM micrographs.

What are Dinoflagellates?

Living dinoflagellates are one of the most important components in plankton. They are small single-celled organisms, which swim freely in water with a forward spiraling motion propelled by dimorphic flagella: one flagellum oriented around the cell, and the other directed posterior. Cells have plates as a cell covering, and numerous cellular structures: chloroplasts mitochondria and nucleus, which set them apart from other groups of land plants belonging to microscopic algae. Many dinoflagellates are primary producers of food in the aquatic food webs. Dinoflagellates are an integral part of the first link in the aquatic food chain: the initial transfer of light energy to chemical energy (photosynthesis). Almost all other organisms are dependent upon this energy transfer for their subsequent existence. This group of microorganisms comprises a large number of unusual algal species of many shapes and sizes.

Importance of Research

In view of the central role dinoflagellates play in marine waters, research is of great importance because of the accelerating pace of environmental degradation worldwide. This effort is aimed at developing state-of-the-art digitized images of marine specimens in the Museum's extensive collections. This site will illustrate the surface of specimens of minuscule, unicellular, marine plants in digitized images. Image-rich pages will include a wealth of morphological information of species taken at high magnifications (1000 to 5000 x) with the SEM. This instrument allows the identification of a group of organisms that are in critical need understanding their biodiversity in oceans.

How to Identify Species?

There are several criteria and morphological terminology used in dinoflagellate species identifications (See figures to right). Life cycle features are very important, and all stages, when known, play a part in recognition of species.

Figure A: Lateral view of a desmokont cell type
Figure B: Ventral view of a dinokont cell type

Cell size and shape are obvious features used, as well as surface ornamentation (pores, spines, ridges, etc.). Another distinction is cell type: desmokont (two dissimilar flagella inserted apically) (Figure A); and dinokont (two dissimilar flagella inserted ventrally) (Figure B). Armored or thecate species are those that possess a multi-layered cell wall, can be distinguished from unarmored or athecate species, those that lack a cell wall.

Orientational terminology is used in describing dinoflagellates. The end pointing forward when the cell moves is called the apical pole (Figure E); the opposite end is the antapical pole (Figure F). Desmokonts are laterally flattened species with two large lateral plates: right valve and left valve (Figure A). In dinokonts the side that the flagella arise from is the ventral side and the opposite side is dorsal (Figure B). These terms are also used in describing the side that the cell is being viewed from. The most characteristic view, except in highly flattened species, (e.g. Prorocentrum sp.), is the ventral view of armored species including the apical pore structure (Figure C) (e.g. Protoperidinium) (Figure E), and the ventral view of unarmed species (Figure D). Additionally, the morphology of the epitheca, cingulum, sulcus (SL), and hypotheca are also important (Figure C & D).

Figure C and D
Figure C: Ventral view of a thecate peridinioid cell
Figure D: Ventral view of an athecate gymnodinoid cell
Figure E and F
Figure E: Apical view of epithecal plates
Figure F: Antapical view of hypothecal plates

Other features used in species descriptions include position of the cingulum and whether it is displaced or not. If displaced and the left side is more anterior, the displacement is left-handed. If the opposite is true, it is right-handed. The former is much more common. The degree of displacement is given in cingulum widths (Figure C & D). In armored species the plate pattern, or tabulation, is crucial for proper identification (Figure C). The description of new species or any critical taxonomy requires complete elucidation of the plate pattern (which can be difficult, requiring special techniques (Figure E & F).

Characters used identifying dinoflagellate species

At the ultrastructural level, dinoflagellates have a common cell covering. In the thecated species the plate pattern is crucial, along with their morphological, flagellar and cytological characters. The identification of new species or any critical taxonomy requires complete elucidation of the plate pattern, apical pore plate, periflagellar area, and cell size and shape which can be difficult, and requiring special techniques. The theca can be smooth ornamented and relatively unornamented. The architectural details of species are complex and species specific. Examples illustrate the surface ornamentation and architectural details of dinoflagellates below.

Protoceratium reticulatum has a round to oval shape and species-specific theca strongly reticulated with pore at the center of each ridged reticulation. The plates are difficult to see without breaking up the theca.

Prorocentrum - CB sp. has a round lenticular shape, compressed in side view. The thecal surface is laced by round to ovoid areolae with smooth margin. Some areolae have oblong trichocyst pores present at the center.

Gambierdiscus australes are round in apical view and compressed anteroposteriorly. The apical pore plate is oriented ventrally. It is an ellipsoid plate with a characteristic large fishhook-shaped apical opening surrounded by rows of evenly distributed round pores on the smooth valve.

Prorocentrum compressum broadly ovate cell in valve view; compressed in side view. The periflagellar area has five characteristic anterior projections, an extension of the periflagellar plates, like collars. Valves covered with evenly distributed round pores situated in depressions.

The cell shape of Prorocentrum gracile is slender that is more than twice as long as broad. It is distinguished by having a long winged anterior spine adjacent to the periflagellar area. Valve covered by evenly distributed round areolae.

The periflagellar area of Prorocentrum sp. is located on the right valve. It is a V---shaped, broad triangle. It has a prominent curved apical collar located adjacent (on the left) to the flagellar pore and a smaller protuberant apical plate (on the right) adjacent to the flagellar pore. The cell has unique valve margins composed of large trichocyst pores which align the cell's margin.

Benthic Species

Prorocentrum mexicanum
Prorocentrum mexicanum- a red tide forming species.
Scrippsiella tifida
Scrippsiella tifida
Scrippsiella tifida
Scrippsiella tifida
Prorocentrum sp.
Prorocentrum sp.
Prorocentrum
Prorocentrum CB-Lair (left) & CB-TW (right).

Ecology

Majority of dinoflagellates (90 %) are marine plankton. They have adapted to the pelagic environment as free-floating in the water column, and to the benthic habitat as attached and associated with the bottom from arctic to tropical seas, from freshwater to estuaries and to hypersaline waters. Many species are cosmopolitan and can live in a variety of habitats: in the plankton, examples of species illustrated as oceanic species; or attached to sediments, sand, corals, or to macroalgal surfaces or to other aquatic plants as illustrated as benthic species present in oceanic coral reef-mangrove habitats. Some species are associated with marine invertebrates and fish. Some even serve as symbionts, known as zooxanthellae, providing organic carbon to their hosts: reef-building corals, sponges, clams, jellyfish, anemones and squid. This group of unicellular microorganisms comprises a large number of unusual algal species of many shapes and sizes. About 140 genera in this group with about 2000 photosynthetic and 2000 heterotrophic species are described.

Oceanic Species

Prorocentrum compressum
Prorocentrum compressum
Protoperidinium crassipes
Protoperidinium crassipes
Protoperidinium mediterraneum
Protoperidinium mediterraneum
Prorocentrum gracile
Prorocentrum gracile
Ornithocercus thumii
Ornithocercus thumii
Podolampas elegans
Podolampas elegans
Ceratochoris horrida
Ceratochoris horrida
Ornithocercus magnificus
Ornithocercus magnificus

What is a Red tide?

Dinoflagellates have attracted much attention from the general public throughout history. The most dramatic effect of dinoflagellates on their environment occurs in coastal waters. An upwelling occurs in the ocean, bathing the surface plankton in nutrients from the bottom of the ocean, or land runoff triggers a 'bloom" of photosynthetic dinoflagellates, whose population density may reach several million per liter of water. 'Blooms' are cell population explosion, may cause discoloration of the water golden or red, and is called 'red tide' (due to accumulation of carotenoid pigments). 'Red tides', can have harmful effects on the sea life and their consumers and species known to form red tides in coral reef mangrove habitats, are illustrated. Toxic Blooms More intriguing and of public concern are the toxins that certain species produce. When these toxic species are in bloom conditions they can cause mass mortalities in a variety of marine organisms. The toxins can be quickly carried up the food chain and indirectly passed onto humans via fish and shellfish consumption, sometimes resulting in gastrointestinal illness, permanent neurological damage, or even death. Socioeconomic stresses also result due to the closing of commercial fisheries and mariculture until the harmful algal bloom dissipates. Over the last several decades many areas of the world, including the United States, have experienced a growing trend in the incidence of toxic dinoflagellate blooms. There are different types of harmful dinoflagellate blooms.

Red Tide Forming

Prorocentrum
Prorocentrum CB-Lair and CB-TW
Prorocentrum sp. red tide producing species enclosed in a thin membrane
Prorocentrum sp. red tide producing species enclosed in a thin membrane
Plagodinium belizeanum
Plagodinium belizeanum producing red tides. Cell shows the presence of two flagella
Prorocentrum arenarium
Prorocentrum arenarium

Toxin Producing Species

Gambierdiscus australes
Gambierdiscus australes
Lingulodinium polyedrum
Lingulodinium polyedrum
Protoceratium reticulatum
Protoceratium reticulatum
Prorocentrum arenarium
  • Species which produce basically harmless nuisance conditions (odors and/or discoloration of water) in sheltered bays and can cause oxygen depletion e.g. Gonyaulax polygramma.
  • Species that produce potent toxins that can find their way through the food chain to humans, causing a variety of gastrointestinal and neurological illnesses. Some species can contaminate shellfish at very low cell concentrations. a). Diarrhetic Shellfish Poisoning (DSP); e.g. Dinophysis acuta, D. acuminata, D. fortii, D. norvegica, D. mitra, D. rotundata, Prorocentrum belizeanum, P. faustiae, P. lima. b). Ciguatera Fish Poisoning; e.g. Gambierdiscus toxicus, Ostreopsis mascarenensis, Prorocentrum sp. Examples of some toxins producing dinoflagellates are illustrated in the SEM photographs. c) Paralytic Shellfish Poisoning (PSP); e.g. Alexandrium acatenella, A. catenella, A. cohorticula, A. fundyense, A. fraterculua, A. minutum, A. tamarense, Gymnodinium catenatum, Pyrodinium bahamense var. compressum. d). Neurotoxin Shellfish Poisoning (NSP); e.g. Karenina breve, K. cf. breve (from New Zealand).
  • Species which are nontoxic to humans but harmful to fish and marine invertebrates, especially in intensive aquaculture systems. The cells may cause damage or clog the gills of these animals; e.g. Gymnodinium mikimotoi.

Summary

Toxins may affect marine fish and birds; e.g., neurotoxins associated with blooms along the west coast of Florida caused mortalities of endangered manatees in 1996. Some blooms are spatially extensive and prevail, while others are patchy and episodic. Toxic blooms have long occurred in some regions, such as along the west coast of Florida and the extended coastlines of Maine and Alaska, while others have developed only in recent years. While harmful dinoflagellate blooms, in a strict sense, are a completely natural phenomena, which have occurred throughout recorded history, in the past two decades the public health and economic impacts of such events appear to have increased in frequency, intensity and geographic distribution. Blooms now threaten virtually every coastal state, cover greater expanses of our coastlines, and involve a multitude of species worldwide.

The microscopic planktonic algae of the world's oceans are critical food for filter-feeding bivalve shellfish (oysters, mussels, scallops, clams) as well as the larvae of commercially important crustaceans and finfish. Therefore, in most cases, the proliferation of plankton algal blooms (up to millions of cells per liter) is beneficial for aquaculture and wild fisheries operations. However, in some situations, algal blooms can have a negative effect, causing severe economic losses to aquaculture, fisheries and tourism operations and having major environmental and human health impacts. In addition to risks to human health and natural resources, significant economic losses regularly result from closure of fisheries and beaches to protect human health: $7 million from a single PSP outbreak in Maine; $25 million from closures related to an NSP outbreak in North Carolina; and $20 million per event from loses to the tourist industry and local governments for Florida red tides.

Glossary

Credits

All images of dinoflagellates were taken by Maria A. Faust using the Philips ESEM at the NMNH SEM Lab with the assistance of Scott Whittaker. I thank Dr. W. John Kress for his continued encouragement and support of marine dinoflagellate research in Belize. Special thanks to Dr. Klaus Ruetzler for introducing her to the magnificent world of coral reef-mangrove ecosystems and for the support from the Caribbean Coral Reef Ecosystem program. This is an inclusive study of aquatic microscopic research that was supported by funds of the Smithsonian Institution.

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