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 Biology and Ecology of Marine Life

BIOLOGY AND ECOLOGY

OF TOXIC PUFFERFISH

Ramasamy Santhanam, PhD

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Library of Congress Control Number: 2017952487

Library and Archives Canada Cataloguing in Publication

Santhanam, Ramasamy, 1946-, author

Biology and ecology of toxic pufferfish / Ramasamy Santhanam, PhD.
(Biology and ecology of marine life)
Includes bibliographical references and index.
Issued in print and electronic formats.
ISBN 978-1-77188-439-6 (hardcover).--ISBN 978-1-315-36601-2 (PDF)
1. Puffers (Fish). 2. Puffers (Fish)--Ecology. I. Title. II. Series: Santhanam, Ramasamy,
1946- . Biology and ecology of marine life.
QL638.T32S28 2017 597'.64 C2017-905677-8 C2017-905678-6

CIP data on file with US Library of Congress

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BIOLOGY AND ECOLOGY OF
MARINE LIFE BOOK SERIES

Series Author:
Ramasamy Santhanam, PhD
Former Dean, Fisheries College and Research Institute,
Tamil Nadu Veterinary and Animal Sciences University,
Thoothukkudi-628 008, India
Email: [email protected]

Books in the Series:

• Biology and Ecology of Toxic Pufferfish
• Biology and Ecology of Venomous Marine Snails
• Biology and Ecology of Venomous Stingrays
• Biology and Culture of Portunid Crabs of the World Seas
• Biology and Ecology of Edible Marine Gastropod Molluscs
• Biology and Ecology of Edible Marine Bivalve Molluscs
CONTENTS

List of Abbreviations ................................................................................... ix

About the Author ......................................................................................... xi
Preface ...................................................................................................... xiii

1. Introduction ................................................................................................ 1
2. Toxic Pufferfish: Biology and Ecology ..................................................... 9
3. Profile of Toxic Pufferfish ........................................................................ 17
4. Pufferfish Toxins ..................................................................................... 275
5. Pufferfish Poisoning ............................................................................... 285
6. Pufferfish Aquariums ............................................................................. 301
7. Diseases and Parasites of Pufferfish and Their Management ............ 319
8. Nutritional Values of Pufferfish ............................................................ 359
9. Pharmaceutical Values of Pufferfish Toxins ........................................ 375
References ................................................................................................ 383
Index ......................................................................................................... 403
LIST OF ABBREVIATIONS

ABC airway breathing, and circulation

DHA docosahexaenoic acid
EAC ehrlich ascites carcinoma
ELISA enzyme-linked immunosorbent assay
EPA eicosapentaenoic acid
FDA Food and Drug Administration
FEHD Food and Environmental Hygiene Department
GH general hardness
GI gastrointestinal
IRL Indian River Lagoon
IUCN International Union for Conservation of Nature
IWT International Wex Technology
LC least concern
MST mean survival time
MTV male-territory-visiting
MU mouse units
ORAC oxygen radical absorbance capacity
PFP puffer fish poisoning
PSP paralytic shellfish poisoning
PST paralytic shellfish toxins
PUFA polyunsaturated fatty acids
SG specific gravity
SL standard length
SPFP saxitoxin pufferfish poisoning
STX saxitoxin
TAA total amino acid
TPFP tetodotoxin pufferfish poisoning
TPNNV tiger puffer nervous necrosis virus
TTX tetrrodotoxin
UV ultraviolet
x List of Abbreviations

VER viral encephalopathy and retinopathy

VGSC voltage-gated sodium channels
VNN viral nervous necrosis
ABOUT THE AUTHOR

Ramasamy Santhanam, PhD

Former Dean, Fisheries College and Research
Institute, Tamilnadu Veterinary and Animal
Sciences University, Thoothukudi, India

Dr. Ramasamy Santhanam is the former Dean of

the Fisheries College and Research Institute at the
Tamilnadu Veterinary and Animal Sciences University in Thoothukudi,
India. His fields of specialization are marine biology and fisheries environ-
ment. Presently he is serving as a resource person for various universities
in India. He has also served as an expert for the Environmental Manage-
ment Capacity Building Technical Assistance Project, a World Bank-aided
project of the Department of Ocean Development, India. He was a mem-
ber of the American Fisheries Society, the World Aquaculture Society, the
Global Fisheries Ecosystem Management Network (GFEMN), and the
International Union for Conservation of Nature’s (IUCN) Commission on
Ecosystem Management, Switzerland. Dr. Santhanam has published 20
books on fisheries science/marine biology as well as 70 research papers.
PREFACE

Pufferfish (also known as blowfish, swellfish or globefish) (family: Tetra-

odontidae) are believed to be the second most poisonous vertebrates in the
world, after the golden poison frog. A total of 197 species of pufferfish
have so far been recorded from the marine, brackish and freshwater habi-
tats of the tropical to sub-tropical regions around the world. The poison-
ous nature of these pufferfish is largely due to the tetrodotoxin (TTX) and
paralytic saxitoxin content of their internal organs viz. liver, ovary, intes-
tine, skin, etc. Tetrodotoxin is a potent neurotoxin, specifically blocking
voltage-gated sodium (Na) channels on the surface of nerve membranes.
It has been reported that the internal organs of almost all the species of
pufferfish contain tetrodotoxin, which is 100 times more potent than cya-
nide, and one puffer fish contains enough toxin to kill 30 adult men. The
muscle portion of some species of pufferfish, which is free of toxin how-
ever, is used to prepare a delicious meal (called fugu in Japan) by specially
trained/licensed chefs in China, Japan, Taiwan and Korea. Further, owing
to their beautiful colorations of the body, many species of pufferfish are
of great use in freshwater, brackish and marine aquariums. TTX is also a
promising source in the development of new drugs. The drug Tetrodin,
obtained from the highly purified TTX, has been reported to mitigate the
sufferings of cancer patients, and it is found that it is 3,000 times more
potent than the pain-killer morphine, without the crippling side-effects of
addiction and nausea.
A thorough understanding about the diversity, biology and ecology of
pufferfish would largely improve the public health community’s ability
to better manage and to prevent pufferfish poisonings. Although several
books on hazardous marine animals are available, a comprehensive book
on the pufferfish of the world seas and other aquatic bodies is still want-
ing. Aspects such as biology and ecology of pufferfish; profile of world’s
marine, brackish and freshwater pufferfish species; characteristics of TTX
and STX of pufferfish; pufferfish poisoning and their symptoms, treat-
ment and management; aquarium uses of pufferfish; and nutritional and
xiv Preface

pharmaceutical values of pufferfish are dealt with in this publication with

suitable illustrations. It is hoped that this publication would be of great use
for the students of fisheries science, marine biology, aquatic biology and
environmental sciences; as a standard reference for all the libraries of col-
leges and universities and as a guide for seagoers and divers.
I am highly indebted to Dr. S. Ajmal Khan, Professor (Emeritus), Cen-
tre of Advanced Study in Marine Biology, Annamalai University, Parangi-
pettai, India, for his valued comments and suggestions on the manuscript.
I am very much grateful to all my international friends who were very
kind enough to provide me with certain photographs of pufferfish at the
time of need. I also thank Mrs. Albin Panimalar Ramesh for her secre-
tarial assistance and help with photography.
CHAPTER 1

INTRODUCTION

CONTENTS

1.1 Introduction about Pufferfish ........................................................... 1

Keywords .................................................................................................. 7

1.1 INTRODUCTION ABOUT PUFFERFISH

Pufferfish (Order: Tetraodontiformes; Family: Tetraodontidae) are com-

monly called as balloonfish, blowfish, bubblefish, globefish, swellfish,
toadfish, and toadies and sea squab. These fishes are generally believed
to be the second-most poisonous vertebrates in the world, after the golden
poison frog. They are the ancient fishes emerging from coral-dwelling
species about 40 million years ago. Well-known saltwater species of the
pufferfish of the Tetraodontiformes are the Porcupinefish (Diodontidae
family), Boxfish (Ostraciidae family), Filefish (Monacanthidae family),
and the Triggerfish (Balistidae family).
Diversity and Distribution: A total of 197 species of pufferfish
(including 2 new species) have so far been recorded. With regard to the
taxonomy of this group, a lot of confusions prevail due to synonyms.
Pufferfish are basically ubiquitous in tropical and sub-tropical waters.
Some live in the extreme shallow waters, while others may range down
to several hundred feet deep (Hanley III, http://www.qualitymarine.com/
News/Species-Spotlight/Puffer-Fish). Majority of the pufferfish (i.e.,
112 species) live in a marine environment and are found worldwide in
the Atlantic, Pacific, and Indian Oceans in a belt of about 47 degrees
north to 47 degrees south latitude in the coastal regions of tropical and
2 Biology and Ecology of Toxic Pufferfish

warm seas including coral reefs or seagrass beds. Though most of the
marine puffers are found in coastal regions, some are oceanic (e.g.,
Lagocephalus lagocephalus) or live in the deep sea (e.g., Sphoeroides
pachygaster). Interestingly, puffers are relatively uncommon in the tem-
perate zone and completely absent from cold waters. Only 37 species are
truly freshwater pufferfish and 48 species are in brackish water (http://
animal-world.com/encyclo/fresh/Puffers/Pufferfish.php. Animal-World.
Pet and Animal Information.). The brackish water species are found
primarily in estuaries, where river mouths meet the ocean. Some will
enter periodically for feeding or breeding, and possibly stay as juveniles,
while others spend their entire lives in brackish conditions. Freshwa-
ter species occur in Amazonia, in tropical Africa, in eastern India and
Southeast Asia (Puffer Fish Facts: http://www.snorkelingpattaya.com/
blog/fish/puffer-fish.html).
Chief Taxonomical Characteristics of Pufferfish: Pufferfish range
in size from the 2.5-centimeter-long dwarf, pea or pygmy puffer to the
freshwater giant puffer, which can grow to more than 60 centimeters in
length. They normally have the appearance of a large tadpole, with bulg-
ing eyes and an elongated snout. They may be found in a variety of colors
but can sometimes be hard to identify when they are not inflated. All the
tetraodontids possess robust, oval-shaped bodies and are characterized by
a tough skin that is often covered with small spinulous scales, a beak-like
dental plate (four large teeth, fused into an upper and lower plate) divided
by a median suture, a slit-like gill opening anterior to the base of the pecto-
ral fin, no pelvic fins, no fin spines, a single usually short-based dorsal fin,
a single usually short-based anal fin, and no ribs. Pufferfish are generally
divided into two groups: the short-nosed puffers (family Tetraodontinae)
and the long-nosed puffers (family Canthigasterinae) (http://www.diveg-
allery.com/pufferfish.htm).
Locomotion: Unlike more typical fish, the body of the pufferfish is
rigid. Hence, it largely relies on its fins for motion and balance. It is
driven mainly by the pectoral fins, dorsal fin and anal fin. Caudal pedun-
cle and caudal fin serve as a rudder. Thus, the puffer is indeed quite slow,
but extremely agile. It can both forward and backward swim and climb
up and down.
Introduction 3

Adaptations: Pufferfish have an unusual defense mechanism – expand-

ing into an enormous ball if threatened. They deploy a special valve in their
mouths to suck water or air into a pleated stomach, expanding up to 3 times
their normal size (http://www.seafocus.com/species_pufferfish.html).
Diet: Pufferfish are omnivorous animals and eat a variety and plants
and animals. They mainly feed on the algae that grow on the rocks and
coral and also the invertebrates that inhabit these areas. Large species of
pufferfish will also eat shellfish such as shrimp and crabs and molluscs.
Breeding: Pufferfish have unique breeding methods. The male puff-
erfish guides the female pufferfish towards the shore where she releases
between 3 and 7 eggs. The eggs of the puffer fish are extremely light and
float on the surface of the water until they hatch in about a week’s time.
The fry are still not fully developed and have a hard shell that protects
them until their limbs begin to grow. The shell of the baby pufferfish then
cracks off and the tail and fins develop. When the puffer fish is big enough,
it will swim down and integrate itself into its reef community.
Use as Food Fish: The skin and internal organs such as liver, ovary,
testis and intestine of many pufferfish species like Takifugu poecilonotus,
T.pardalis, T.vermicularis, T.chrysops and T.rubripes are highly toxic to
humans, but nevertheless the meat of some species is considered a deli-
cacy in Japan (as fugu) and Korea (as boh-guh) (http://memim.com/tetra-
odontidae.html). According to Chinese,
“No food is tasty after eating the puffer.”
“The man that eats fugu is stupid; the man that does not eat fugu is also
stupid.” (Cohen and Law-Yone, http://www.imagequest3d.com/pages/gen-
eral/news/puffertoxin/; https://www.travelblog.org/Asia/Japan/Okinawa/
Camp-Kinser/blog-305533.html).
The pufferfish meat that exceeded the regulatory limit of 2 μg.g–1 (10
MU·g–1) TTX as established by the by the Japan Food Hygiene Associa-
tion (2005) is not considered safe for human consumption. This calls for
removing TTX to ensure the safe consumption of pufferfish (Mohamad,
2013; Nuñez-Vazquez et al., 2012). In this book, the toxic and less toxic
puffers have been considered as ‘poisonous to eat’ and ‘ harmless’ species,
respectively. In the former (poisonous to eat) pufferfish species, the safe
level (2 μg.g–1) of TTX exceeds in their meat and the whole fish is unfit for
human consumption. On the other hand, in the harmless species, after the