Phylum Cnidaria (Formerly Coelenterata) Has Been Reported to Be Responsible for More Envenomations Than Any Other Marine Phylum

Home , Aglaopheniidae, Air fern, Alatinidae, Atorella, Carukiidae, Catostylidae

Ramasamy Santhanam

Biology and Ecology of Venomous Marine Cnidarians Biology and Ecology of Venomous Marine Cnidarians Ramasamy Santhanam

Biology and Ecology of Venomous Marine Cnidarians Ramasamy Santhanam Fisheries College and Research Institute Tamil Nadu Veterinary and Animal Sciences University Thoothukudi, Tamil Nadu, India

ISBN 978-981-15-1602-3 ISBN 978-981-15-1603-0 (eBook) https://doi.org/10.1007/978-981-15-1603-0

# Springer Nature Singapore Pte Ltd. 2020 This work is subject to copyright. All rights are reserved by the Publisher, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilms or in any other physical way, and transmission or information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed. The use of general descriptive names, registered names, trademarks, service marks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. The publisher, the authors, and the editors are safe to assume that the advice and information in this book are believed to be true and accurate at the date of publication. Neither the publisher nor the authors or the editors give a warranty, expressed or implied, with respect to the material contained herein or for any errors or omissions that may have been made. The publisher remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

This Springer imprint is published by the registered company Springer Nature Singapore Pte Ltd. The registered company address is: 152 Beach Road, #21-01/04 Gateway East, Singapore 189721, Singapore Preface

Seas and oceans cover 70% of the earth’s surface. While the plants of these ecosystems produce 70% of the oxygen we breathe, their deep waters are home to 80% of all life found on the planet. So far about 250,000 species have been collected and formally described from these systems. Among the different components of marine life, the phylum Cnidaria (formerly Coelenterata) has been reported to be responsible for more envenomations than any other marine phylum. It is believed that 2% of about 11000 species are toxic to humans. Accidents caused by jellyfish are common all around the world, with serious manifestations and occasional deaths reported in some countries. The major species of jellyfish associated with accidents in Brazil include the cubozoans Tamoya haplonema and Chiropsalmus quadrumanus; and the hydrozoans Portuguese man-of-war, Physalia physalis and Olindias sambaquiensis. While the first two species are responsible for both local and systemic signs and symptoms, P. physalis causes severe injuries to bathers and fishermen. O. sambaquiensis provokes mild accidents on the southeastern coast. Though books such as Poisonous and Venomous Marine Animals of the World, Biology and Ecology of Venomous Marine Scorpionfishes, Biology and Ecology of Venomous Marine Snails and Biology and Ecology of Toxic Pufferfish are presently available on venomous marine fauna, a comprehensive book on the Biology and Ecology of Venomous Marine Cnidarians (formerly coelenterates) has not so far been published. This publication, the first of its kind, would answer this long felt need. It deals with the biology, ecology, envenomations, venomology and treatment and management of 240 species of marine cnidarians. It is hoped that the present publication when brought out would be of great use as a standard text-cum-reference for researchers, teachers and students of various disciplines such as fisheries science and marine biology; as a guide for beach goers, divers, physicians and environmentalists; and as a valuable reference book for libraries of colleges and universities. I am highly indebted to Dr. K.Venkataramanujam, former dean, Fisheries College and Research Institute, Tamil Nadu Veterinary and Animal Sciences University, Thoothukudi, India, for his valued comments and suggestions on the manuscript. I sincerely thank all my international friends who were very kind enough to collect

v vi Preface and send certain species/images of venomous marine cnidarians for the present publication. The services viz. photography and secretarial assistance rendered by Mrs. Albin Panimalar Ramesh are also gratefully acknowledged.

Thoothukudi, India Ramasamy Santhanam Contents

1 Introduction ...... 1 1.1 Ecology of Marine Cnidarians ...... 2 1.2 Envenomation of Marine Cnidarians ...... 2 1.2.1 Irukandji Syndrome ...... 2 1.2.2 Marine Cnidarian Envenomations that Cause Severe Injuries in Humans ...... 3 1.2.3 Cnidarian Toxins ...... 3 1.2.4 Harm to Fisheries ...... 3 1.2.5 Uses of Cnidarians ...... 4 2 Biology of Marine Cnidarians [Phylum Cnidaria (¼ Coelenterata)] ...... 7 2.1 Biology of the Hydrozoans (Hydroids) (Class Hydrozoa) ...... 7 2.1.1 Geographic Range ...... 8 2.1.2 Habitat ...... 8 2.1.3 Anatomy ...... 8 2.1.4 Nervous System ...... 10 2.1.5 Communication and Perception ...... 10 2.1.6 Behaviour ...... 10 2.1.7 Food Habits ...... 10 2.1.8 Predation ...... 11 2.1.9 Defence Mechanism ...... 11 2.1.10 Reproduction ...... 11 2.1.11 Ecosystem Roles ...... 12 2.1.12 Signiﬁcance to Humans ...... 12 2.2 Biology of the True Jellyﬁsh (Scyphomedusae) (Class Scyphozoa) ...... 13 2.2.1 Characteristics of Scyphozoa ...... 13 2.2.2 Distribution ...... 14 2.2.3 Habitat ...... 14 2.2.4 Size ...... 14 2.2.5 Colouration ...... 14 2.2.6 Biology ...... 15

vii viii Contents

2.3 Biology of the Box Jellyﬁsh (Cubomedusae) (Class Cubozoa) . . . 18 2.3.1 Distribution ...... 18 2.3.2 Habitat ...... 19 2.3.3 Behaviour ...... 19 2.3.4 Physical Characteristics ...... 19 2.3.5 Feeding Ecology and Diet ...... 19 2.3.6 Reproductive Biology ...... 20 2.3.7 Signiﬁcance to Humans ...... 20 2.4 Biology of the Anthozoans (Anemones) (Class Anthozoa) ...... 20 2.4.1 Distribution ...... 21 2.4.2 Habitat ...... 21 2.4.3 Formation of Coral Reefs ...... 21 2.4.4 Biology of Anthozoa ...... 21 2.4.5 Association ...... 26 2.4.6 Predators ...... 26 2.4.7 Bioluminescence ...... 27 2.4.8 Lifespan ...... 27 2.4.9 Coral Reefs and Their Uses ...... 27 2.4.10 Environmental and Commercial Importance ...... 27 3 Biology and Ecology of the Venomous Marine Hydrozoans (Class Hydrozoa) ...... 29 3.1 Family: Aeginidae ...... 29 3.2 Family Aequoreidae ...... 31 3.3 Family Aglaopheniidae ...... 34 3.4 Family Apolemiidae ...... 39 3.5 Family Corynidae ...... 40 3.6 Family Cuninidae ...... 41 3.7 Family Eirenidae ...... 42 3.8 Family Geryoniidae ...... 43 3.9 Family Haleciidae ...... 44 3.10 Family Hydractiniidae ...... 46 3.11 Family Milleporidae ...... 48 3.12 Family Olindiidae ...... 54 3.13 Family Pandeidae ...... 59 3.14 Family Pennariidae ...... 62 3.15 Family Physaliidae ...... 63 3.16 Family Porpitidae ...... 65 3.17 Family Rhizophysidae ...... 68 3.18 Family Rhopalonematidae ...... 70 3.19 Family Sertulariidae ...... 72 Contents ix

4 Biology and Ecology of the Venomous Marine True Jellyﬁsh (Class Scyphozoa) ...... 75 4.1 Family Atollidae ...... 75 4.2 Family Cassiopeidae ...... 78 4.3 Family Catostylidae ...... 81 4.4 Family Cepheidae ...... 84 4.5 Family Cyaneidae ...... 86 4.6 Family Drymonematidae ...... 90 4.7 Family Linuchidae ...... 91 4.8 Family Lobonematidae ...... 93 4.9 Family Lychnorhizidae ...... 94 4.10 Family Mastigiidae ...... 95 4.11 Family Nausithoidae ...... 97 4.12 Family Paraphyllinidae ...... 97 4.13 Family Pelagiidae ...... 98 4.14 Family Periphyllidae ...... 113 4.15 Family Rhizostomatidae ...... 114 4.16 Family Stomolophidae ...... 123 4.17 Family Ulmaridae ...... 125 5 Biology and Ecology of the Venomous Marine Box Jellyﬁsh (Class Cubozoa) ...... 133 5.1 Family Alatinidae ...... 133 5.2 Family Carukiidae ...... 137 5.3 Family Carybdeidae ...... 145 5.4 Family Chirodropidae ...... 153 5.5 Family Chiropsalmidae ...... 158 5.6 Family Chiropsellidae ...... 162 5.7 Family Tamoyidae ...... 163 5.8 Family Tripedaliidae ...... 166 6 Biology and Ecology of the Venomous Marine Anthozoans (Class Anthozoa) ...... 169 6.1 Family Acroporidae ...... 169 6.2 Family Actiniidae ...... 173 6.3 Family Actinodendridae ...... 218 6.4 Family Agariciidae ...... 221 6.5 Family Aiptasiidae ...... 222 6.6 Family Alcyoniidae ...... 226 6.7 Family Aliciidae ...... 228 6.8 Family Andvakiidae ...... 233 6.9 Family Corallimorphidae ...... 235 6.10 Family Diaduminidae ...... 236 6.11 Family Discosomidae ...... 240 6.12 Family Edwardsiidae ...... 242 x Contents

6.13 Family Exocoelactinidae ...... 245 6.14 Family Gorgoniidae ...... 246 6.15 Family Halcuriidae ...... 247 6.16 Family Hormathiidae ...... 249 6.17 Family Metridiidae ...... 252 6.18 Family Nephtheidae ...... 254 6.19 Family Parazoanthidae ...... 256 6.20 Family Phymanthidae ...... 257 6.21 Family Plexauridae ...... 258 6.22 Family Pocilloporidae ...... 260 6.23 Family Sagartiidae ...... 261 6.24 Family Sphenopidae ...... 262 6.25 Family Stichodactylidae ...... 268 6.26 Family Thalassianthidae ...... 279 6.27 Family Xeniidae ...... 283 6.28 Family Zoanthidae ...... 284 7 Venomology of Marine Cnidarians ...... 287 7.1 Venom Apparatus in Marine Cnidarians ...... 287 7.1.1 Mechanism of Cnidae Discharge ...... 288 7.1.2 Venom Apparatus in Sea Anemones ...... 289 7.2 Characteristics of Marine Cnidarian Venoms ...... 289 7.2.1 Enzymes ...... 290 7.2.2 Pore-Forming Toxins ...... 291 7.2.3 Neurotoxins (Voltage-Gated Ion Channel Toxins) . . . . . 292 7.2.4 Non-protein Bioactive Components ...... 293 7.3 Envenomation of Marine Cnidarians ...... 294 7.3.1 Venomous Species of Cnidaria ...... 294 7.3.2 Envenomation ...... 295 7.3.3 Main Stinging Cnidarians ...... 297 7.3.4 Jellyﬁsh Envenomation and Irukandji Syndrome ...... 298 7.3.5 Sea Anemone Envenomation ...... 300 7.3.6 Globally Recorded Jellyﬁsh Stings ...... 301 7.4 Treatment and Management of Marine Cnidarian Envenomations ...... 304 7.4.1 Treatment and Management of Scyphozoan Stings . . . . . 305 7.4.2 Treatment of Cubozoan Envenomation ...... 307 7.4.3 Therapeutic Approaches to Injuries Caused by Sea Anemone Stings ...... 311 7.4.4 Treatment of Venomous Hydrozoans ...... 314 Contents xi

7.5 Therapeutic Potential of Venom of Marine Cnidarians ...... 315 7.5.1 Role of Cnidarians Venoms in Drug Discovery ...... 315 7.5.2 Hydrozoan Venoms Possessing Therapeutic Activities ...... 316 7.5.3 Scyphozoan Venoms Possessing Therapeutic Activities ...... 316 7.5.4 Cubozoan Venoms Possessing Therapeutic Activities . . . 317 7.5.5 Anthozoan Venoms Possessing Therapeutic Activities . . . 318

References ...... 321 Index ...... 335 About the Author

Ramasamy Santhanam is the former dean of the Fisheries College and Research Institute, Tamil Nadu Veterinary and Animal Sciences University (now the Tamil Nadu Dr. J. Jayalalithaa Fisheries University), India. He has 50 years of teaching and research experience in marine sciences, and his fields of specialization include marine biology and fisheries environment. He presently serves as a fisheries expert for various government and nongovernment organizations in India and abroad. Dr. Santhanam has published 29 books on various aspects of marine life, marine plankton and aquaculture. He was a member of the American Fisheries Society, United States; World Aquaculture Society, United States; Global Fisheries Ecosys- tem Management Network (GFEMN), United States; and the IUCN’s Commission on Ecosystem Management, Switzerland.

xiii Introduction 1

The seas and oceans cover ~70% of the earth’s surface and contain 80% of all life found on the planet. It is estimated that they supply two-thirds of the value of all the natural services provided by our natural environment. The range of goods and services provided by these resources include fisheries, shipping routes, oxygen (half of the world’s supply), CO2 sink (by absorbing more than 50 times than atmosphere), temperature and weather control and water cycle which are integral parts of our health and economies and even our weather. It is also estimated that about half of the world’s population lives within the coastal zone, and the economic benefits generated by the seas and oceans per year is 2.5 trillion US$—only slightly less than the world’s total GNP (Anon. 2009, http://www.grida.no/resources/5612, 2010, http://www.protectplanetocean.org/collections/introduction/introbox/oceans/ introduction-item.html). However, it is saddening to note that these seas and oceans also serve as home for thousands of species of venomous creatures such as cnidarians (formerly coelenterates), snails, fishes and rays which are threatening human lives. Among these animals, the organisms of phylum Cnidaria are considered very important owing to their envenomation. While most of the cnidarians are found in marine environments approximately 40 species, mostly hydrozoans, live in freshwater (Jouiaei et al. 2015a, b). The phylum Cnidaria which is with a total of about 11,000 species has about 200 (~2%) potentially dangerous species to humans. This phylum includes true jellyfish (class Scyphozoa, 200 spp., 2%), box jellyfish (class Cubozoa, 50 spp., less than 1%), sea anemones and corals (class Anthozoa, 7500 spp., 68%) and hydroids (class Hydrozoa, 2700 spp., 30%) (Hale 1999; Rocha et al. 2011). However, the World Register of Marine Species database recorded 10,762 cnidarian species.

# Springer Nature Singapore Pte Ltd. 2020 1 R. Santhanam, Biology and Ecology of Venomous Marine Cnidarians, https://doi.org/10.1007/978-981-15-1603-0_1 2 1 Introduction

1.1 Ecology of Marine Cnidarians

Marine cnidarians are living in various habitats worldwide and they range in size from less than 1 cm in length to the massive lion’s mane jellyfish, Cyanea capillata with the bell diameter exceeding 2 m. In polar waters some scyphozoan species can reach bell diameters of about 3 m and have tentacles of 43 m long (Anon. https:// projects.ncsu.edu/project/bio402_315/new%20cnidaria/Untitled-2016.html). Warmer oceans, agriculture runoff, commercial fishing and the creation of artificial reefs may have an impact on increased numbers of the cnidarians in recent years (Inman 2018). The geographic distribution of jellyfish also seems to be undergoing an impact by global warming.

1.2 Envenomation of Marine Cnidarians

The global problem of marine envenomation is not fully understood. Each year hundreds of deaths occur by envenomation (stinging) by jellyﬁsh. The morbidity is even greater with jellyﬁsh stings worldwide being numbered in their millions. In each summer it is estimated that up to half a million stings occur on the east coast of the USA due to the hydrozoan Portuguese man-o’-war (Physalia physalis). Large numbers of stings also occur on the east and west coasts of both South Africa and Australia, where some 20,000+ stings have been reported to occur each year. In New Zealand waters, there are three main stinging species, viz. Physalia physalis, Cyanea sp. and Apolemia uvaria.

1.2.1 Irukandji Syndrome

Most notorious feature of cubozoans is their extremely dangerous venom (Tibballs et al. 2012). Most species within this class can cause medically significant stings, and this class includes the world’s most venomous marine creature, Chironex fleckeri, which can kill an adult human within minutes. Most box jellyfish prefer calm tropical and subtropical near-shore marine habitats, areas that are frequently shared with tourists, fishermen, surfers and divers. The syndrome which occurs after envenomation by a tiny carybdeid box jellyfish in tropical Australian waters in summer months is called the “Irukandji syndrome”. There are about 16 known species of Irukandji, of which Carukia barnesi, Malo kingi, Malo maxima, Malo filipina and Malo bella are the best known (https://en.wikipedia.org/wiki/Irukandji_ syndrome). Jellyfish species responsible for similar envenomation include a tiny hydroid (jellyfish), Gonionemus present in the Japan Sea and other large carybdeid species worldwide, the sand jellyfish Stomolophus nomurai in the China Sea and Physalia physalis (Portuguese/Pacific man-o’-war) worldwide (Fenner 1997). 1.2 Envenomation of Marine Cnidarians 3

1.2.2 Marine Cnidarian Envenomations that Cause Severe Injuries in Humans (Mizuno et al. 2012)

A. Jellyfishes Portuguese man-of-war, Physalia physalis Irukandji jellyfish, Carukia barnesii, Malo kingi Mauve stinger, Pelagia noctiluca Box jellyfish, Chironex fleckeri Chesapeake Bay sea nettle, Chrysaora quinquecirrha Sea wasp, Chiropsalmus quadrigatus

B. Fire coral Millepora alcicornis

C. Sea anemones The Hell’s Fire sea anemone, Actinodendron plumosum Night sea anemone, Phyllodiscus semoni Haddon’s carpet anemone, Stichodactyla haddoni Snakelock’s anemone, Anemonia sulcata (¼Anemonia viridis) Condylactis sp. Source: Mizuno et al. (2012)

1.2.3 Cnidarian Toxins

Cnidarians possess a wide variety of biologically active substances that can be considered as toxins. Anthozoan toxins can be classiﬁed into two chemically very different groups, namely polypeptide toxins isolated from sea anemones and diterpenes isolated from octocorals. Cubozoan and scyphozoan protein toxins have been the most elusive cnidarian toxins to investigate—despite a tremendous effort in the past few decades, very few of these large, relatively unstable protein toxins were isolated, but recently this has been achieved for cubozoan venoms. Hydrozoans mainly contain large proteins with physiological mechanisms of action similar to the sea anemone and jellyﬁsh pore-forming toxins (Mizuno et al. 2012).

1.2.4 Harm to Fisheries

Large aggregations of the following species of medusa have been reported to hinder trawl ﬁshing in coastal waters of several locations worldwide by clogging nets, thereby these medusa have caused economic losses to ﬁsheries (Nagata et al. 2009).

Olindias sambaquiensis Chrysaora lactea Chiropsalmus quadrumanus 4 1 Introduction

Lychnorhiza lucerna Tamoya haplonema Rhacostoma atlantica Phyllorhiza punctata

1.2.5 Uses of Cnidarians

1.2.5.1 Edible Values Some species of jellyfish in the Rhizostomae order caught in coastal areas have been utilized in China, as a source of food and ingredient in Chinese cuisine for over 1700 years. Cannonball jellyfish (Stomolophus meleagris) and jelly blubber (Catostylus mosaicus) are edible species of jellyfish. Rhopilema esculentum and Rhopilema hispidium are edible jellyfish and are the most common ones consumed in China, Japan and Korea. Additional edible jellyfish species include Aurelia aurita, Crambionella orsini, Chrysaora pacifica, Lobonema smithi, Lobonemoides gracilis and Stomolophus nomuria. Desalted ready-to-use jellyfish are low in calories and contain hardly any fat, about 5% protein and 95% water. In some areas of Asia, jellyfish is “associated with easing bone and muscle pain”. Jellyfish is consumed in several Asian and Southeast Asian countries. In 2001, it was reported that Japan had annually imported between 5400 and 10,000 tons of edible jellyfish from Indonesia, Malaysia, Myanmar, the Philippines, Singapore, Thailand and Vietnam. Dehydrated and pickled jellyfish is considered a delicacy in several Asian countries, including China, Korea, Taiwan, Vietnam and Japan. A preparation method using dehydrated jellyfish involves re-hydrating the product by soaking it in water for several hours and then parboiling, rinsing and slicing it (Anon. https://en.wikipedia.org/wiki/ Jellyfish_as_food).

1.2.5.2 Insecticide The freshwater jellyﬁsh Craspedacusta sowerbii is presently used in biological control of mosquitoes as an alternative to insecticide (Dodson and Cooper 1983). During recent decades, the interest for the biology and utilization of marine cnidarians has grown and a number of bioactive compounds (secondary metabolites) with anticancer and antioxidant activities have been isolated in the interest of human health. These compounds offer vast scope as sources in the development of new drugs (Mariottini and Pane 2014).

1.2.5.3 Role of Marine Cnidarian Venoms in Drug Discovery Research ﬁndings have demonstrated that the cnidarian toxins may provide promising sources of pharmacological lead/active agents for therapy of human diseases. Palytoxin isolated from certain marine species including Zoantharia coral has been reported for anticancer activity against head and neck carcinoma cells, Ehrlich ascites tumour and P-388 lymphocytic leukaemia cells. Equinatoxin II (EqT II) is a pore-forming protein that has been shown to have signiﬁcant toxicity against 1.2 Envenomation of Marine Cnidarians 5

Ehrlich ascites tumour and L1210 leukaemia cell lines and diploid lung fibroblasts of the Chinese hamster. Equistatin is a potent inhibitor of papain-like cysteine proteinase and aspartic proteinase cathepsin D. Antibutyrylcholinestrasic activity of the crude venom has been extracted from the Mediterranean jellyfish Pelagia noctiluca. Inhibition of butyrylcholinesterase in the central nervous system may be useful in the treatment of neurodegenerative diseases such as Alzheimer’s disease and senile dementia. ShK is a potent Kv1.3 channel blocker toxin that isolated from the sea anemone Stoichactis helianthus. Since this channel is crucial in the activation (proliferation and cytokine production) of human effector memory T cells (TEM), ShK could provide a valuable immunosuppressant for the treatment of autoimmune diseases. Further, Kv1.3 blockers are also considered as a therapeutic target for the treatment of obesity and insulin resistance. About 2000 active molecules have been isolated from the marine cnidarians between 2000 and 2010. Some of these compounds have been used in traditional medicines to treat hypertension, respiratory, genitourinary, dermatological, neurological and haematological diseases. To date, however, none of the identified compounds extracted from cnidarians have been effectively developed as drugs. Although, pseudopterosin extracted from the sea whip Pseudopterogorgia elisabethae, Eleutherobin from Eleutherobia sp. (soft coral) and Erythropodium caribaeorum and Sarcodictyns from some corals have been investigated in preclini- cal studies (Jouiaei et al. 2015a; Mariottini and Grice 2016). Biology of Marine Cnidarians [Phylum Cnidaria (¼ Coelenterata)] 2

2.1 Biology of the Hydrozoans (Hydroids) (Class Hydrozoa)

Among the marine invertebrates, the oldest extant group is the marine phylum Cnidaria, which includes true jellyﬁsh (class Scyphozoa), box jellyﬁsh (class Cubozoa), sea anemones and corals (class Anthozoa) and hydroids (class Hydrozoa).

Box jelly Moon jelly Anemone Physalia

Classes and animals of phylum Cnidaria

Image courtesy: Marine Education Society of Australasia The Hydrozoa is a class of the Phylum Cnidaria with about 3700 species. Hydrozoans (Class Hydrozoa) are small solitary and colonial animals, and most of them are marine in their habitats. A few genera (like Hydra) which live in fresh water

# Springer Nature Singapore Pte Ltd. 2020 7 R. Santhanam, Biology and Ecology of Venomous Marine Cnidarians, https://doi.org/10.1007/978-981-15-1603-0_2 8 2 Biology of Marine Cnidarians [Phylum Cnidaria (¼ Coelenterata)] are solitary, and most of the marine species are colonial. Colonial hydrozoans include siphonophore colonies, Hydractinia, Obelia and many others. The colonies of the colonial species can be large, and in some cases the specialized individual animals cannot survive outside the colony. Better-known marine hydrozoans include Portuguese man-o-wars (Physalia physalis), by-the-wind sailors (Velella velella), ﬁre coral (Milleporidae), air fern (Sertularia argentea) and pink-hearted hydroids (Tubularia).

2.1.1 Geographic Range

Marine hydrozoans are found in all the oceans, at all latitudes (tropical, temperate and polar).

2.1.2 Habitat

Marine hydrozoans are found in nearly all marine habitats, except perhaps heavy surf zones. They are most abundant and diverse in warm shallow waters.

2.1.3 Anatomy

Most hydrozoan species include both a polypoid and a medusoid stage in their lifecycles, although a number of them have only one or the other. For example, the freshwater Hydra has no medusoid stage, while the marine Liriope lacks the hydroid stage.

Polyps: The hydroid form is usually colonial, with multiple polyps connected by tube-like hydrocauli. The hollow cavity in the middle of the polyp extends into the associated hydrocaulus so that all the individuals of the colony are intimately connected. Where the hydrocaulus runs along the substrate, it forms a horizontal root-like stolon that anchors the colony to the bottom. The colonies are generally small, no more than a few centimetres across, but some in Siphonophores (Physalia) can reach sizes of several metres. They may have a tree-like or fan-like appearance, depending on species. The polyps themselves are usually tiny, although some non-colonial species are much larger, reaching 6–9 cm or in the case of the deep- sea Branchiocerianthus, it is 2 m. The hydrocaulus is usually surrounded by a sheath of chitin and proteins called the perisarc. In some species, this extends upwards to also enclose part of the polyps, in some cases including a closeable lid through which the polyp may extend its tentacles. In any given colony, the majority of polyps are specialized for feeding. These have a more or less cylindrical body with a terminal mouth on a raised protuberance called the hypostome, surrounded by a number of tentacles. The polyp contains a central cavity, in which initial digestion takes place. All colonial hydrozoans also include some polyps specialized for reproduction. 2.1 Biology of the Hydrozoans (Hydroids) (Class Hydrozoa) 9

These lack tentacles and contain numerous buds from which the medusoid stage of the lifecycle is produced. The arrangement and type of these reproductive polyps vary considerably between different groups.

Medusae: The medusae of hydrozoans are smaller than those of typical jellyﬁsh (scyphozoans), ranging from 0.5 to 6 cm in diametre. Although most hydrozoans have a medusoid stage, this is not always free-living, and in many species, exists solely as a sexually reproducing bud on the surface of the hydroid colony. The body of a medusa consists of a dome-like umbrella ringed by tentacles. A tube-like structure hangs down from the centre of the umbrella and includes the mouth at its tip. Most hydrozoan medusae have just four tentacles, although a number of exceptions exist. Stinging cells are found on the tentacles and around the mouth. The mouth leads into a central stomach cavity. Four radial canals connect the stomach to an additional, circular canal running around the base of the bell, just above the tentacles.

A hydrozoan polyp

Structure of a hydromedusa 10 2 Biology of Marine Cnidarians [Phylum Cnidaria (¼ Coelenterata)]

2.1.4 Nervous System

It is unusually advanced for cnidarians. Two nerve rings lie close to the margin of the bell of the medusa, and send ﬁbres into the muscles and tentacles. The genus Sarsia has even been reported to possess organized ganglia. Numerous sense organs are closely associated with the nerve rings. Mostly these are simple sensory nerve endings, but they also include statocysts and primitive light- sensitive ocelli.

2.1.5 Communication and Perception

All hydrozoans have tactile and chemical-sensing structures. Some also have eyespots that detect light and/or statocysts that detect gravity. They communicate mainly by chemical signals. Some free-swimming hydrozoans, including many siphonophores, have bioluminescent structures. It is unlikely that they communicate with other hydrozoans (their light sensors are too simple for this). Possibly they are lures for prey.

2.1.6 Behaviour

Hydrozoans combine sessile or sedentary polyp stages and free-swimming solitary stages in their life cycles. Some can move by crawling, but most are sessile. The siphonophores form ﬂoating colonies. Many free-swimming hydrozoans follow the diel migration pattern common to many pelagic marine organisms. They spend daylight hours in deep water where light does not penetrate, and rise to the surface after sunset.

2.1.7 Food Habits

Hydrozoans vary in their feeding habits. Many trap small zooplankton with their tentacles. Some filter suspended particles (such as fish eggs and foecal pellets) from the water column. Some consume phytoplankton. A few groups contain symbiotic algae, and may get most of their nutritional needs from their symbionts. Pelagic hydrozoans, including siphonophore colonies and medusae, are known to show 2.1 Biology of the Hydrozoans (Hydroids) (Class Hydrozoa) 11 some selectivity in prey types, some taking mainly fish larvae, others taking soft- bodied invertebrates, others micro-crustaceans.

2.1.8 Predation

Hydrozoans are preyed by many types of predators. A variety of snails and worms graze on polyps and stolons, as do some ﬁsh and crustaceans. Fish also consume medusae and pelagic colonial hydrozoans, as do some sea turtles (especially leatherbacks), ctenophores and other cnidarians, including larger hydrozoans. Most hydrozoan medusae also follow the diel migration pattern common to many planktonic organisms—sinking below the limit of light penetration to avoid visual predators during the day, and then rising towards the surface at night in pursuit of prey.

2.1.9 Defence Mechanism

Nearly all hydrozoans protect themselves with their cnidocysts (cnidae). Some colonial species have specialized polyps that grow large tentacles armed with dense batteries of these stinging cells or grow large rigid spines.

2.1.10 Reproduction

Hydrozoans are mostly broadcast spawners. Polyps reproduce asexually by budding, creating daughter polyps, medusae or both. In some species medusae reproduce asexually as well, by ﬁssion or budding. Medusae (if present in the life cycle) or polyps produce gametes. Most hydrozoan species are dioecious, a few are sequential hermaphrodites. Eggs and sperm are most often released into the water column and fertilization is external. In some species, eggs are retained and fertilized internally, in which case embryos may be released as larvae or retained until even more developed. Eggs and sperm are released into the water, and left to survive on their own. In a few species, eggs are retained in special structures on the parent, and the embryos are retained as brood, developing to the planula or even young polyp stage. 12 2 Biology of Marine Cnidarians [Phylum Cnidaria (¼ Coelenterata)]

Life cycle of hydrozoans

2.1.11 Ecosystem Roles

Hydrozoans are both predators and prey for many marine organisms, and large seasonal blooms of medusae may strongly affect local ﬁsh and zooplankton populations. Some species of polyps are hosts for symbiotic algae, and many large pelagic forms have symbiotic hyperiid amphipods living on or in them. There is even a small species of ﬁsh, Nomeus gronovii, that lives in association with Portuguese man-o-wars. Some polyp colonies grow on the shells of hermit crabs, providing them protection.

2.1.12 Significance to Humans

Hydrozoans are important parts of many marine food chains. Species of the families Milleporidae and Stylasteridae that have colonies with calcareous exoskeletons are harvested commercially. There are now limits on their trade and some are considered 2.2 Biology of the True Jellyfish (Scyphomedusae) (Class Scyphozoa) 13 endangered. However, the stings of some hydrozoans (most famously the Portu- guese man-o'-war, Physalis physalis) are dangerous to humans. Also, the ﬁre corals (Mille-poridae) do harm to the divers if they touch them. Hydrozoans are also common members of “fouling communities”—the benthic organisms that naturally attach to hard substrates and so grow on the hulls of ships and on submerged water pipes, interfering with their function.

2.2 Biology of the True Jellyfish (Scyphomedusae) (Class Scyphozoa)

The class Scyphozoa which includes true jellyﬁsh (or “true jellies”) are exclusively marine. These scyphozoans live in all oceans, from the Arctic to tropical waters. They consist of 96% water and range in diametre from 2 cm to 2 m. This class includes 4 orders, 20 families, 66 genera and about 200 species (Anon. 2019; Waggoner et al. 1994) and is currently divided into the following four orders viz.

1. Order Stauromedusae—These stalked jellyfish are sessile cup-shaped forms and lack a free-swimming medusa. 2. Order Coronatae—These crown or grooved jellyfish are mostly deep-dwelling jellyfish and are rarely seen. 3. Order Semaeostomae—These disc jellyfish include the most common as well as the largest of the jellyfish. 4. Order Rhizostomae—These jellyfish lack tentacles and have eight highly branched, oral arms.

2.2.1 Characteristics of Scyphozoa (Santhanam and Srinivasan 1994; Anon. http://scyphozoans.tripod.com/)

1. These are large, soft-bodied, gelatinous marine invertebrates that swim by contracting their umbrella-shaped swimming bell. 2. They exhibit radial symmetry, i.e. the body parts are arranged symmetrically around a central point. 3. They are diploblastic, i.e. their body wall is composed of two layers, an ectoderm and an endoderm separated by the mesoglea. 4. They have stinging cells (cnidae) which contain a barbed thread-like projectile and are used to attack and paralyse their prey. 5. They undergo alternation of generations and reproduce both sexually and asexually resulting in the production of both polyps and medusae. However, the medusae predominate. 6. These scyphozoans possess a gastrovascular cavity (coelenteron) functioning in digestion and as a ﬂuid transport system, hydrostatic skeleton, brood chamber and kidney. 14 2 Biology of Marine Cnidarians [Phylum Cnidaria (¼ Coelenterata)]

2.2.2 Distribution

The scyphozoans inhabit every ocean in the world and are capable of withstanding a wide range of salinity and temperature. Most stauromedusae are found in cool waters along temperate to sub-polar shorelines spring through autumn. Coronate medusae generally occur at great depths, where temperatures are a cool 40–46 F(5–8 C), but a few species occur in subtropical to tropical waters. Semaeostome species are the predominant large medusa in polar to temperate oceans, and they also inhabit subtropical and tropical waters. The scyphistomae of those species are active only in warm months; however, they may become dormant and survive through winter months. Rhizostome species live mostly in tropical waters, with only a few species found in subtropical or temperate regions. The medusae of shallow-living scyphozoans are seen during late spring to early autumn in surface waters of temperate to polar seas. In tropical waters and among deep-dwelling species, medusae may be present all year.

2.2.3 Habitat

Most jellyﬁsh live in shallow coastal waters, but a few species inhabit depths of 4600 m (Arai 1997) and their polyps are found attached to hard surfaces, such as pilings, shells and rocks, at various depths, depending on the species. Most Stauromedusae are seen mainly at intertidal areas. Coronate medusae typically are found at mesopelagic depths (500–1500 m), but a few species occur near the surface. Deep-living species may have polyps at abyssal depths, but the polyps of shallow- living species are on shallow substrates. Semaeostome and rhizostome medusae occur most abundantly near shore in surface waters above 150 m, where food supplies are greatest. Their polyps also are found at shallow depths, often on the underside of structures away from direct light. Some semaeostome species are deep living, and their polyps generally are not known. There are no known deep-dwelling rhizostome species.

2.2.4 Size

Jellyﬁsh range in size from a mere 12 mm to more than 2 m across, the largest is Cyanea capillata (¼ Cyanea arctica) which may have tentacles over 40 m long (Mayer 1910).

2.2.5 Colouration

Some scyphozoans are coloured due to their gonads or other internal structures. Bell of some species is deeply pigmented. 2.2 Biology of the True Jellyfish (Scyphomedusae) (Class Scyphozoa) 15

2.2.6 Biology

Most species of Scyphozoa have two life history phases, including the planktonic medusa or jellyﬁsh form, which is most evident in the warm summer months, and an inconspicuous, but longer-lived, bottom-dwelling polyp, which seasonally gives rise to new medusae.

2.2.6.1 Anatomy The scyphozoans invariably display a four-part symmetry and have an internal gelatinous material called mesoglea, which serves as a skeleton. The mesoglea includes mobile amoeboid cells originating from the epidermis. These animals have no hard parts, including no head, no skeleton and no specialized organs for respiration or excretion. The mouth opens into a central stomach, from which four interconnected diverticula radiate outwards. In many species, this is again elaborated by a system of radial canals, with or without an additional ring canal towards the edge of the dome. Some genera, such as Cassiopea, even have additional, smaller mouths in the oral arms. The lining of the digestive system includes further stinging nematocysts, along with cells that secrete digestive enzymes (Santhanam et al. 2015).

A scyphozoan medusa—subumbrella view

2.2.6.2 Behaviour Jellyfish behaviour generally is simple, owing to their simple nervous system. Stauromedusae move around on the substrate by somersaulting, which they accom- plish by alternating adhesion of the basal disc with that of tentacles or adhesive pads located between the tentacles of some genera. The most noticeable behaviour of 16 2 Biology of Marine Cnidarians [Phylum Cnidaria (¼ Coelenterata)] jellyfish is the rhythmic pulsation of the swimming bell, which moves them through the water for feeding and respiration. The swimming pulsations are coordinated by nerve centres around the edge of the bell. At the bell margin, there also are sensory clubs (rhopalia), each consisting of a light-sensing organ (ocellus) and a gravity- sensing organ (statocyst). Using these organelles, these medusae can sense light and dark and can determine their orientation in the water column. Semaeostome and rhizostome jellyfish swim continuously. This is important for oxygen exchange and for feeding. The swimming of several species of jellyfish is known to be against flow in the water column and as a result, all the jellyfish swim in the same direction and may become concentrated in convergences, like bales of hay stacked up to dry. Some species, however, move up in the water column at night and down in the day (“diel vertical migration”). The scyphistomae (polyps) are able to move by the so-called foot and its extensions.

2.2.6.3 Feeding Ecology and Diet All scyphozoans feed with tentacles or tentacle-like projections that have millions of microscopic intracellular organelles called “nematocysts”. Some nematocysts act to paralyse or kill the prey, whereas others entangle them. Stauromedusae catch prey by the tentacles and fold the arm inward to bring the prey to the mouth. Many coronate medusae do not swim actively while feeding but instead remain nearly motionless with their tentacles extended above the bell. For semaeostome and rhizostome medusae, the pulsations of the swimming bell force water through the tentacles and create vortices that may bring prey into contact with the tentacles and oral arms. For semaeostome medusae, when a prey item is immobilized on a tentacle, the tentacle contracts and transfers the prey to an oral arm. The prey is moved by cilia up the inside of the folded oral arm to the mouth and into one of the four gastric (stomach) pouches, where short, finger-like projections wrap around the prey and secrete digestive enzymes. For rhizostome medusae, prey capture is by the small tentacles on the oral arms, which transfer the prey to one of the many small mouths nearby. Most of the jellyfish species feed on small crustaceans that predominate in most habitats. Stauromedusae consume epibenthic crustaceans, including gammarid amphipods and harpacticoid copepods. Medusae in the other orders of this class Scyphozoa primarily eat abundant calanoid copepods and also eat other small zooplankton, such as cladocerans, larvaceans (¼ appendicularians) and chaetognaths. Many semaeostome species also feed on other gelatinous species, including scyphomedusae, hydromedusae, siphonophores and ctenophores. It is of particular interest that several scyphozoan species are known to consume the eggs and larvae of fish.

2.2.6.4 Reproduction Most species of Scyphozoa have two life history phases, including the planktonic medusa or jellyﬁsh form, which is most evident in the warm summer months, and an inconspicuous, but longer-lived, bottom-dwelling polyp, which seasonally gives rise to new medusae. Most scyphozoan species are gonochorists, i.e. with separate males and females. The gonads are located in the stomach lining, and the mature gametes 2.2 Biology of the True Jellyfish (Scyphomedusae) (Class Scyphozoa) 17 are expelled through the mouth. After fertilization, some species brood their young in pouches on the oral arms, but they are generally leading a planktonic life. The fertilized egg produces a planula larva which, in most species, attaches itself to the sea bottom. This larva develops into the hydroid stage of the lifecycle, a tiny sessile polyp called a scyphistoma which reproduces asexually, producing similar polyps by budding, and then either transforming into a medusa or budding several medusae off from its upper surface by a process called strobilation. These medusae are microscopic and may take years to reach sexual maturity.

Life cycle of a scyphozoan medusa

2.2.6.5 Food Value of Jellyfish In Japan and China, scyphozoan jellyfish are important food and have been exploited for more than 1700 years. In China they are considered a culinary delicacy and are thought to have medicinal value. A multimillion-dollar commercial fishery exists for at least ten species of rhizostome medusae throughout Southeast Asia, and a fishery for Stomolophus Meleagris has been started in the Gulf of Mexico. The swimming bell of the jellyfish is processed in a mixture of salt and alum and packaged for distribution. The semidried jellyfish is rehydrated, desalted, blanched and served in a variety of dishes. The prepared jellyfish has a special crunchy texture.

2.2.6.6 Aquarium Value of Jellyfish Owing to their great beauty and swimming pulsations, scyphozoan jellyfish have been a great success as specimens in public aquariums and even as household pets. Over the past decade, considerable advances have been made in jellyfish husbandry, and several species are on display at aquariums worldwide. In Japan jellyfish are kept as pets in special aquariums (Anon. https://www.encyclopedia.com/plants-and- animals/animals/zoology-invertebrates/jellyfish). 18 2 Biology of Marine Cnidarians [Phylum Cnidaria (¼ Coelenterata)]

2.2.6.7 Jellyfish and Fisheries The jellyfish scyphomedusae of the order Rhizostomeae are fished commercially for food. However, the moon jelly Aurelia aurita of the order Semaeostomeae and the enormous Nemopilema nomurai of the order Rhizostomeae, found between Japan and China, cause major fisheries disruptions. In northern waters, large shoals several kilometres long sometimes hamper fishing by clogging nets (Anon. https://ucmp. berkeley.edu/cnidaria/scyphozoa.html). Fish populations and commercial fisheries may be affected detrimentally by jellyfish. Jellyfish may occur in great abundance, and, if they are caught in fishing nets, their great weight may cause the nets to rip or the fish catch to be damaged. Jellyfish eat the pelagic eggs and larvae of fish as well as the small zooplankton prey of fish larvae and zooplanktivorous fish species. Therefore, jellyfish both eat fish and compete with them for food. Jellyfish also appear to be intermediate hosts for some parasites of fish. Jellyfish have been a nuisance to fish farms, where they break up on the fish impoundments and sting and kill the fish, and to power plants, where they may clog the cooling water intake screens, sometimes causing the plants to suspend operations.

2.2.6.8 Harmful Effects of Jellyfish to Humans Scyphozoan jellyﬁsh have direct and indirect effects on humans, many of which are negative. Swimmers fear them for their painful stings. All jellyﬁsh sting, but the stings of small specimens and those with short tentacles often are not painful to humans. Among the scyphozoans, the genera Chrysaora and Cyanea are known for painful stings but they are not deadly.

2.3 Biology of the Box Jellyfish (Cubomedusae) (Class Cubozoa)

Cubozoans (Class, Cubozoa) which have been derived from Scyphozoa are commonly called as sea wasps or box jellies. Though they are basically similar to the true jellyﬁsh, they can swim pretty fast, maneuvre around things and see fairly well. These organisms can cause serious pain due to the fact that they possess dangerous nematocysts. Chironex ﬂeckeri, Carukia barnesi and Malo kingi are among the deadliest creatures in the world, having caused human fatalities (Anon. https:// ucmp.berkeley.edu/cnidaria/cubozoa.html).

2.3.1 Distribution

Cubozoans can be found in most tropical and subtropical waters. Carybdea marsupialis and Carybdea rastoni have been found in temperate waters as well. 2.3 Biology of the Box Jellyfish (Cubomedusae) (Class Cubozoa) 19

2.3.2 Habitat

The preferred habitat of cubozoans seems to be over sandy substrate, with box jellies located just above the bottom during the day and moving up towards the surface at night.

2.3.3 Behaviour

Cubozoans have the most complex behaviour of any cnidarian. They are active swimmers and are capable of moving 3–6 m per minute. They are positively phototactic (move towards light) and are active during the day and night, although they may feed only during the night or predawn hours. Vision clearly plays a role in both feeding and reproduction. It is reported that these organisms react to the presence of their human observers by swimming away.

2.3.4 Physical Characteristics

The most obvious characteristic of these cuboidal medusae is the box-like shape of their bell. The manubrium and mouth are located inside the bell, and the velarium is along the edge of the bell. Pedalia are muscular extensions of the bell and the tentacles are attached to the pedalium. While chirodropids have multiple tentacles attached to each pedalium, carybdeids have only one tentacle per pedalium. Between the pedalia are the unique sensory structures known as rhopalia. Each rhopalium has a statocyst and six eyes, four simple eyes and two relatively complex eyes. These organisms possess blue-, green- and ultraviolet-sensing opsins in both the small and large complex eyes. The cubomedusan nervous system is complex compared to that of other classes of Cnidaria. A diffuse synaptic nerve net throughout the bell region is connected to a subumbrellar nerve ring, and nerve processes extend from this ring into the rhopaliar stalks (Anon. https://www.encyclopedia.com/environment/ encyclopedias-almanacs-transcripts-and-maps/cubozoa-box-jellies).

2.3.5 Feeding Ecology and Diet

Cubozoans are predators feeding mainly on ﬁshes and crustaceans. Additional prey items include polychaetes, crab megalopae (post-larvae), isopods, amphipods, sto- matopod (“mantis shrimps”) larvae and chaetognaths (arrow worms). As active predators, cubozoans chase, catch and eat ﬁshes and other organisms. Feeding behaviour may vary slightly between species. The prey are caught on the tentacles and brought up towards the pedalia by the tentacle contracting. The medusa then either remains upright in the water or turns upside down. The pedalium with the prey item then bends inward towards the manubrium, and the prey are then engulfed. 20 2 Biology of Marine Cnidarians [Phylum Cnidaria (¼ Coelenterata)]

2.3.6 Reproductive Biology

Little is known about the reproductive biology of cubozoans. The life history of these organisms includes a benthic stage, the polyp, which can reproduce asexually by budding, and a pelagic stage, the medusa. Eggs and sperm combine to form a ciliated larva (planula), which settles on the bottom and becomes a polyp. Unlike the true jellyﬁsh (scyphozoans), cubozoan polyps do not undergo strobilation (asexual reproduction by division into body segments) and the entire polyp becomes the juvenile medusa. Copula sivickisi (¼ Carybdea sivickisi) uses spermatophores that can be stored by the female, and it has been hypothesized that female Carybdea rastoni may collect sperm strands produced by the males. Other cubozoans may have internal fertilization, but most of them broadcast their gametes.

2.3.7 Significance to Humans

The presence of “stinger-resistant enclosures” on beaches in northern Queensland, Australia, is indicative of the impact of cubozoans on humans. Although deaths are reported almost every year from encounters with the most dangerous Chironex ﬂeckeri, the overall impact of cubozoans is much greater as stings are not invariably reported. Further, Carukia barnesi is now recognized as the cause of “Irukandji syndrome”, which results in severe backache, muscle pains, chest and abdominal pains, headache, localized sweating and piloerection (erection or bristling of hairs), as well as nausea and reduced urine output (Anon. https://www.encyclopedia.com/ environment/encyclopedias-almanacs-transcripts-and-maps/cubozoa-box-jellies).

2.4 Biology of the Anthozoans (Anemones) (Class Anthozoa)

Anthozoans (“ﬂower animals”) are exclusively marine and over 6000 solitary and colonial species have been described in this largest class of the phylum Cnidaria or “stinging needles”. In this, there are two main subclasses in the class Hexacorallia, members of which have sixfold symmetry and include the stony corals, sea anemones, tube anemones and zoanthids; and Octocorallia, which have eightfold symmetry and include the soft corals and gorgonians (sea pens, sea fans and sea whips)andsea pansies. The smaller subclass, Ceriantharia, however, consists of the tube-dwelling anemones. These animals do not have a medusa stage in their development and these exclusively polypoid cnidarians are characterized by a tubular body with tentacles around the mouth and most are sedentary after the larval stage (Anon. https://www.newworldencyclopedia.org/entry/Anthozoa). 2.4 Biology of the Anthozoans (Anemones) (Class Anthozoa) 21

2.4.1 Distribution

The anthozoans are found worldwide in all oceans, from the Arctic to the Antarctic. Most species live in warm, tropical waters in coral reef habitats. Reef-building corals are only found in shallow tropical and subtropical waters.

2.4.2 Habitat

Anthozoans are found from intertidal zones to deep ocean trenches of more than 6000 m deep. Species may be solitary or colonial. While solitary forms may attach to a hard substrate or burrowed into soft mud or sand on the sea bed, the colonial forms may build massive skeletons, such as the reef-building corals. However, their larvae can disperse as part of the plankton. Some groups of anthozoans, such as those of the orders Actiniaria (sea anemones), Ceriantharia (tube anemones) and Pennatulacea (sea pens and sea pansies), may show some movement (Anon. https://www. newworldencyclopedia.org/entry/Anthozoa).

2.4.3 Formation of Coral Reefs

The coral reefs are formed by the calcareous skeletons of many generations of coral polyps. These reefs are able to create massive structures like the Caribbean and the Great Barrier Reef. The polyps inhabit only the surface of the reefs. The coral head is actually a colony made up of many small, interconnected anthozoan polyps. These colonies form by asexual reproduction in which the developing bud forms a polyp that remains attached to the parent. Several coral species secrete an exoskeleton as follows. The ectodermal cells at the base of the polyp secrete the cup-shaped exoskeleton called the calicle or basal plate. The basal plate is made up of calcium. As the polyp grows, the calicle size increases and, over time, becomes the major constituent of coral reefs (Anon. https://nationalzoo.si.edu/animals/corals-and-sea- anemones-anthozoa).

2.4.4 Biology of Anthozoa

2.4.4.1 Size Anthozoans range in size from small individuals less than half a centimetre across to large colonies a metre or more in diametre.

2.4.4.2 Colouration Anthozoans include species with a wide range of colours from red, pink and purple to yellow, blue and orange. 22 2 Biology of Marine Cnidarians [Phylum Cnidaria (¼ Coelenterata)]

2.4.4.3 General Characteristics of Anthozoa The anthozoans (corals and anemones) have a body plan characterized by radial symmetry. These animals have a single opening that serves as both the mouth and the anus. Tentacles with stinging structures, called nematocysts, usually surround this opening. There are many subclasses and orders with varying characteristics as detailed below. Subclass Hexacorallia: This subclass is comprising about 4300 species (Anon. https://en.wikipedia.org/wiki/Hexacorallia). These organisms are formed of polyps which are generally with sixfold symmetry. It has five extant orders viz. (i) Actiniaria—sea anemones; (ii) Antipatheria—black corals; (iii) Corallimorpharia—similar to sea anemones; (iv) Scleractinia—stony corals and (v) Zoantharia—zoanthids. The hexacorallia are distinguished from the other subclass, Octocorallia, in having six or fewer axes of symmetry in their body structure; and the tentacles are simple and unbranched and normally number more than eight. These organisms are formed of individual soft polyps which in some species live in colonies and can secrete a calcite skeleton. Order Actiniaria (Sea anemones): Larger anemones tend to be solitary while smaller species may use asexual reproduction to propagate and live in large concentrations when there is suitable habitat. Anemones of this order have a wide range of colours, some owing their colouration to the zooxanthellae, microscopic algae, they host. These anemones have a disc-shaped bottom which they use to attach themselves to rocks, in crevices and on other suitable surfaces, including the shells of other marine invertebrates. Order Antipatharia (Black corals): It is an order of deep water, tree-like corals. Black corals were previously classified in the taxon Ceriantipatharia with the ceriantharians, but they were later reclassified under Hexacorallia. Order Scleractinia (Stony corals): Stony or reef-building corals form a skeleton made of calcium carbonate under the polyps as coral. These corals are responsible for forming the base structure of coral reefs. As older polyps die off, new polyps continue to build calcifications on the old skeletons, thus forming huge reefs. Not all stony corals are reef-building as some are not able to produce enough calcium carbonate to from reef. Order Corallimorpharia (Anemone corals or mushroom corals): Members of this order resemble anemones more closely than other types of corals due to their large, flat, disc-like shape and short tentacles. They grow like wheel spokes, radiating from a centre and forming concentric circles. The diametre of the circle increases as they grow. This order is extremely popular in home aquariums. Order Zoantharia (Zoanthids): These organisms have long, prominent tentacles arranged in two rows. Unlike stony and soft corals, zoanthids incorporate sand and other substrate into their colonies for structure. They may live as individual polyps or in colonial groups. Subclass Octocorallia (also known Alcyonaria) (Octocorals): This subclass is comprising around 3000 species with soft corals, sea pens, gorgonians and sea fans (Anon. https://en.wikipedia.org/wiki/Octocorallia). Though these organisms have a similar appearance with stony corals, they do not build the hard, calcium carbonate skeleton. Instead, these corals may create some internal structural supports that allow 2.4 Biology of the Anthozoans (Anemones) (Class Anthozoa) 23 them to grow vertically but still sway with ocean currents. Soft corals are always colonial and grow with eightfold symmetry, which means their tentacles come in groups of eight—hence the name Octocoral. Subclass Ceriantharia (Tube-dwelling anemones): This subclass looks similar to sea anemones, but tube-dwelling anemones are known for their solitary nature and living buried in soft sediments. They live inside tubes made of secreted mucus and organelles and can recede into these tubes for protection.

2.4.4.4 Physical Characteristics of Polyps The anthozoans have the characteristic gastrovascular cavity which is large and divided by walls or septa. The latter arise as folds from the body wall. These folds, along with the mouth and pharynx, are usually arranged in a biradially symmetric pattern. The basic unit of the adult organism is the polyp, which consists of a cylindrical column topped by a disc with a central mouth surrounded by tentacles. Sea anemones are mostly solitary, but the majority of corals are colonial, formed by the budding of new polyps from an original, founding individual. Colonies are strengthened by calcium carbonate and other materials and take various massive, plate-like, bushy or leafy forms. Anthozoans are essentially a tubular sac, with a mouth and tentacles position around the mouth on a ﬂattened upper surface known as an oral disk. As with other cnidarians, the tentacles surrounding the mouth have stinging cells and the mouth is the only entry to the digestive system. The basic body shape of a cnidarian consists of a sac with a gastrovascular cavity, with a single opening that functions as both mouth and anus. It has radial symmetry, meaning that whichever way it is cut along its central axis (that is, by any plane that passes through its longitudinal axis), the resulting halves would always be mirror images of each other.

2.4.4.5 Anatomy of a Stony Coral Polyp The basic body form of an anthozoan is the polyp. This consists of a tubular column topped by a ﬂattened area, the oral disc, with a central mouth; a whorl of tentacles surrounds the mouth. In solitary individuals, the base of the polyp is the foot or pedal disc, which adheres to the substrate, while in colonial polyps, the base links to other polyps in the colony. The mouth leads into a tubular pharynx which descends for some distance into the body before opening into the coelenteron, otherwise known as the gastrovascular cavity, which occupies the interior of the body. The coelenteron is subdivided by a number of vertical partitions, known as mesenteries or septa. The body wall consists of an epidermal layer, a jelly-like mesogloea layer and an inner gastrodermis. The tentacles of polyps are armed with nematocysts, venom- containing cells. Some sea anemones have a circle of acrorhagi outside the tentacles. Another form of weapon is the similarly armed acontia (thread-like defensive organs) which can be extruded through apertures in the column wall. Many anthozoans are colonial and consist of multiple polyps. The simplest arrangement is where a stolon runs along the substrate in a two-dimensional lattice with polyps budding off at intervals. Alternatively, polyps may bud off from a sheet of living tissue, the coenosarc, which joins the polyps and anchors the colony to the substrate. 24 2 Biology of Marine Cnidarians [Phylum Cnidaria (¼ Coelenterata)]

Anatomy of an anthozoan polyp

2.4.4.6 Food and Feeding Members of most species of Anthozoa are suspension feeders, capturing small planktonic invertebrates, phytoplankton, bacteria and other suspended organic matter. All cnidarian species can feed by catching prey with nematocysts, with large sea anemones capable of catching fish, crabs and bivalves, and corals are capable of catching plankton.Some of the anthozoan species harbour a type of symbiotic algae, dinoflagellates called zooxanthellae. The reef-building corals known as hermatypic corals rely on this symbiotic relationship particularly. The zooxanthellae benefitby using nitrogenous waste and carbon dioxide produced by the host, and the cnidarian gains photosynthetic capability and increased calcium carbonate production in hermatypic corals (Anon. https://www.newworldencyclopedia.org/entry/Anthozoa).

2.4.4.7 Reproduction and Development Unlike other members of this phylum, anthozoans do not have a medusa stage in their development. Corals reach sexual maturity at different ages, varying by species and colony size. Some can mature and reproduce successfully in as little as 4 years, 2.4 Biology of the Anthozoans (Anemones) (Class Anthozoa) 25 while others can take decades to reproduce. Anthozoans can reproduce sexually and asexually. Most anthozoans are unisexual but some stony corals are hermaphrodite. The germ cells originate in the endoderm and move to the gastrodermis where they differentiate. When mature, they are liberated into the coelenteron and subsequently to the open sea, with external fertilization. The zygote develops into a planula larva which swims by means of cilia and forms part of the plankton for a while before settling on the seabed and metamorphosing into a juvenile polyp. Some planulae contain yolky material and others incorporate zooxanthellae, and these adaptations enable these larvae to sustain themselves and disperse more widely.

Stages in Longitudinal Binary fission

Budding in Anthozoa

Asexual reproduction in Anthozoa 26 2 Biology of Marine Cnidarians [Phylum Cnidaria (¼ Coelenterata)]

Sexual reproduction in Anthozoa. (Image courtesy: Richa Shah)

Anthozoans are also capable of a variety of asexual means of reproduction including fragmentation, longitudinal and transverse ﬁssion and budding. For example, sea anemones can crawl across a surface leaving behind them detached pieces of the pedal disc which develop into new clonal individuals. Anthopleura species divide longitudinally, resulting in groups of individuals with identical colouring and patterning. Transverse ﬁssion is less common but occurs in Anthopleura stellula and Gonactinia prolifera. Zoanthids are capable of budding off new individuals. Anthozoans also exhibit great powers of regeneration. In this method lost parts swiftly regrow (Anon. https://nationalzoo.si.edu/animals/corals-and-sea-anemones- anthozoa).

2.4.5 Association

Corals that grow on reefs are called hermatypic, with those growing elsewhere are known as ahermatypic. Most of the ahermatypic corals are azooxanthellate and live in both shallow and deep-sea habitats. In the deep sea they share the ecosystem with soft corals, polychaete worms, other worms, crustaceans, molluscs and sponges. Marine fauna, such as hydrozoa, bryozoa and brittle stars, often live among the branches of gorgonian and coral colonies. The pygmy seahorse, Hippocampus bargibanti, not only makes certain species of gorgonians its home but closely resembles its host and is well camouﬂaged. Some organisms have an obligate relationship with their host species. The mollusc Simnialena marferula is only found on the sea whip Leptogorgia virgulata and the nudibranch, Tritonia wellsi, is another obligate symbiont. A number of sea anemone species are commensal with other organisms. Certain crabs and hermit crabs place sea anemones on their shells for protection; and ﬁsh, shrimps and crabs live among the anemone’s tentacles, gaining protection. Some amphipods live inside the coelenteron of the sea anemone.

2.4.6 Predators

Despite their venomous cells, sea anemones are eaten by ﬁsh, starﬁsh, worms, sea spiders and molluscs. The sea slug Aeolidia papillosa feeds on the aggregating anemone (Anthopleura elegantissima), accumulating the nematocysts for its own protection. 2.4 Biology of the Anthozoans (Anemones) (Class Anthozoa) 27

2.4.7 Bioluminescence

Some species of the subclass Alcyonaria (Octocorrallia) can produce light (biolumi nescence) that may even exhibit as a wave of light across a colony.

2.4.8 Lifespan

It is estimated that most coral reefs are between 5000 and 10,000 years old, with some actually tracing their beginnings back 50 million years. It is unclear how long the lifespan of an individual coral or anemone is (https://nationalzoo.si.edu/animals/ corals-and-sea-anemones-anthozoa).

2.4.9 Coral Reefs and Their Uses

Coral reefs rival rainforests in diversity of life and they hold the most diverse ecosystems on the planet. Living coral reefs cover more than 936,000 km2 and harbour one of every four ocean species known to man, yet they cover less than 0.1% of the entire ocean. They also provide more than a home for ﬁsh and other reef dwellers. These coral reefs act as an important buffer between land and the daily erosion from waves or occasional storm surges. These rich productive habitats also serve as nursery grounds for the juvenile stages of ocean life. Coral reefs also support the tourist industry and a strong ﬁshing industry. Organisms found on coral reefs have provided key ingredients for innumerable medical compounds that treat every- thing from asthma and cancer to HIV and still show potential for future pharmaceutical discoveries (https://nationalzoo.si.edu/animals/corals-and-sea-anemones- anthozoa).

2.4.10 Environmental and Commercial Importance

Anthozoans are of great use for human beings in a number of ways. Coral reefs are major tourist attractions and also provide a habitat for ﬁsh, mollusks, urchins and crustaceans that serve as food for people. Anthozoans are used in the aquarium trade, to make coral jewellery, and scleractinian skeletons are even used as building materials and in bone grafts. Despite these values, various human activities (ﬁshing, development, marine pollution) have had negative effects on coral reefs, with more than half of the world’s coral reefs considered to be threatened (Anon. https://www. newworldencyclopedia.org/entry/Anthozoa). Biology and Ecology of the Venomous Marine Hydrozoans (Class Hydrozoa) 3

3.1 Family: Aeginidae

Aegina citrea Eschscholtz, 1829

Common name (s): Four tentacled jelly Global distribution: Tropical; cosmopolitan; Antarctic, Atlantic, Pacific and Arctic Oceans. Ecology: This pelagic, reef-associated species is commonly found in lagoon areas at depths of about 3–8 m; it is an active swimmer tolerating brackish water conditions; depth range is 0–1600 m. Biology Description: This hydrozoan jellyfish has an umbrella which is slightly more conical than hemispherical. Jelly is thick at apex and flattened orally. Stomach is large and circular with eight rectangular stomach pouches. There are four to six tentacles, and their roots are large, recurved apically, penetrating deep into central

# Springer Nature Singapore Pte Ltd. 2020 29 R. Santhanam, Biology and Ecology of Venomous Marine Cnidarians, https://doi.org/10.1007/978-981-15-1603-0_3 30 3 Biology and Ecology of the Venomous Marine Hydrozoans (Class Hydrozoa) mesoglea. Deep exumbrellar grooves are present above and below tentacles and are with nematocyst-laden floor and sides. Colour of the tentacles, stomach and stomach pouches is yellow in live condition. Maximum diameter of the umbrella is 50 mm. Food and feeding: This jellyfish like other cnidarians is generally carnivorous feeding on planktonic organisms, crustaceans, small fish, fish eggs and larvae and other jellyfish. Predators: The ctenophore Haeckelia rubra readily eats the tentacles of this medusa. Life cycle: This species has been listed only in medusoid stage. Envenomation: The extracts of this species have shown haemolytic activity (breaking down of red blood cells—erythrocytes, causing anaemia) (Mariottini 2014).

Aeginura grimaldii Maas, 1904

Common name (s): Narcomedusa Global distribution: Polar, subtropical and boreal; Atlantic, Pacific and Arctic Oceans: Mexico, Brazil, Canada and USA. Ecology: This deep sea, pelagic jellyfish has a depth range of 0–1600 m. Biology Description: Umbrella of this beautiful jellyfish is up to 10 cm. Manubrial pouches have slight secondary division. There are three to five secondary marginal tentacles in each octant; and one or two statocysts between each secondary tentacle. Mouth stalk is absent; mouth leads to a big stomach. Gonads are in the wall of the stomach. Colour of manubrium is deep chocolate to purplish black. Food and feeding: It is a predator feeding mainly on gelatinous zooplankton. Predators: The predators of this species include physonect siphonophores, ctenophores and cephalopods. 3.2 Family Aequoreidae 31

Life cycle: In this species, two life cycles are occurring simultaneously: (1) asexual budding of actinula larvae from the parent medusa which develop into a fully developed medusa; and (2) sexual reproduction producing an egg and phorocyte pair which develops into an actinula and a four-tentacle reduced medusa. Envenomation: The extracts of this species induced haemolytic activity (breaking down of red blood cells—erythrocytes, causing anaemia) in sheep RBC (Mariottini 2014).

3.2 Family Aequoreidae

Aequorea forskalea Peron & Lesueur, 1810 (¼ Aequorea aequorea; Medusa aequorea)

Common name (s): Water jelly, crystal jelly, many-ribbed jellyﬁsh Global distribution: Subtropical south-east Atlantic and eastern Paciﬁc; off the west coast of North America Ecology: This pelagic, coastal to offshore species is usually found offshore in waters deeper than 150 m. Biology 32 3 Biology and Ecology of the Venomous Marine Hydrozoans (Class Hydrozoa)

Description: Adult umbrella of this species is large and saucer-shaped and is thick in centre, gradually thinning towards margin. Stomach is usually half as wide as disc. Radial canals (usually 60–160) are dark brown or bluish. They are with gonads along almost their whole length. Tentacles which are long and delicate usually fewer than radial canals but varied. Marginal bulbs are few, scattered; tentacle bulbs are elongated and conical. It is a brightly luminescent bioluminescent jellyfish, capable of producing flashes of blue light. It is harvested for its luminescent aequorin, used in neurological and biological experiments to detect calcium. It can live more than 2 years. Food and feeding: These jellies feed primarily on soft-bodied prey including other jellyfishes, ctenophores and appendicularians. They can expand their mouths when feeding to swallow jellies more than half their size. Envenomation: It is a mild stinging jellyfish (Anon. http://lifecubomed.es/media/ cms_page_media/1/Cubomed%20guide_2014.pdf). According to some researchers, its cnidocysts (stinging cells) are not dangerous for humans, making it one of the most harmless species of jellyfish.

Aequorea globosa Eschscholtz, 1829

Image credit: # 2018 Riek, Denis Common name (s): Crystal jelly Global distribution: Tropical; temperate; Indo-west Paciﬁc and west Indian Ocean; Indonesia. Ecology: It is a pelagic, neritic species; depth range is 0–210 m. Biology Description: Umbrella which is almost hemispherical is 20–40 mm wide, and mesoglea is very thick. Stomach is about half as wide as the diameter of umbrella; velum is narrow; mouth is simple and circular and gastric peduncle is absent. There are 40–48 radial canals which are with smooth margin. Gonads are extending along almost the entire length of the radial canals. There are 30–38 tentacles. Envenomation: This is a mildly stinger jellyﬁsh (Anon. http://www.cmas.org/ news/watch-out-for-the-gelatinous-organisms-of-the-eastern-mediterranean). 3.2 Family Aequoreidae 33

Aequorea vitrina Gosse, 1853

Common name (s): Crystal jelly, disk jellyfish, lampshade. Global distribution: Subtropical north-east Atlantic: England; Denmark, North Sea, British Isles, The Channel, French and Spanish Atlantic coast; sparse around mainland Scotland. Ecology: This is a coastal, pelagic species. Biology Description: Umbrella of this species is saucer-shaped, thick in centre and is gradually thinning towards margin. Stomach is about half the width of the disc. Radial canals are 60–100 in number, and gonads are extending along almost their entire length. Tentacles are more than three times as numerous as radial canals and are with a few small marginal bulbs which are elongated and are slightly laterally compressed, with excretory papillae. Colour of the animal is violet-blue fluorescent. It attains a maximum umbrella diameter of 20 cm. Food and feeding: In stagnant water this species remains stationary with its very long (about 4Â bell diameter) marginal tentacles which are motionless hanging down in the water and are ready for ambush capture of prey organisms. It is found to be efficient at capturing brine shrimps (Artemia salina) and is less efficient at capturing rotifers (Brachionus plicatilis). Both the bell margin and the mouth move towards each other so that the captured prey can be transferred from the tentacle to the elongated mouth-lips to be further transported into the mouth and stomach where digestion takes place. This is bioluminescent due to its luminescent protein, aequorin and the associated fluorescent molecule green fluorescent protein (GFP). Envenomation: This jellyfish is a mild stinger (Anon. http://www.cmas.org/news/ watch-out-for-the-gelatinous-organisms-of-the-eastern-mediterranean). 34 3 Biology and Ecology of the Venomous Marine Hydrozoans (Class Hydrozoa)

3.3 Family Aglaopheniidae

Aglaophenia cupressina Lamouroux, 1816

Image credit: FrédéricDucarme, French Wikipedia. Common name (s): Stinging hydroid, feather hydroid. Global distribution: Tropical Indo-Paciﬁc; western Indian Ocean. Ecology: This sessile species lives on shallow reefs with moderate current; depth range is 1–43 m. Biology Description: This species has feather-like projections with plumose branches and side branches. Its colour may vary from green to brown/grey and its size may vary from 20 to 50 cm. Food and feeding: It is ﬁlter feeder on zooplankton. Predators: This species is preyed by several species of nudibranchs. Life cycle: These animals reproduce sexually and a planula larva results. This larval form is blown by currents to a suitable reef surface and attaches, becoming a new branching colony. Envenomation: It has a powerful sting (Anon. http://www.peerintoyourworld. com/species/aglaopheniidae/aglaophenia-cupressina-stinging-hydroid/). Contact with stinging hydroid may lead to some pain and a rash in the area that will irritate the victim for 10 days (Sutton 2016). 3.3 Family Aglaopheniidae 35

Aglaophenia pluma Linnaeus, 1758

Image courtesy: Shutterstock Common name (s): Podded hydroid, toothed feather hydroid Global distribution: Subtropical Pacific: New Caledonia, Korea, USA and Canada. Ecology: This sessile, shallow-water species lives intertidally from the shore to 120 m under water. It often grows on the brown alga Halidrys siliquosa; on rock and gravel, Sargassum spp. and occasionally on stipes of Laminaria spp. It is the only Aglaophenia likely to be found in rock pools or on the shore. Biology Description: These are upright colonial hydroids with stems which may grow to 3–4 cm in total height by 1 cm wide. Its central stem bears alternating unbranched side branches with polyps all facing upwards. Each feeding polyp is surrounded by three defensive polyps. The reproductive polyps are enclosed in a basket-like corbula, which replaces a normal side branch. Colony is brown in colour. Food and feeding: This species is suspensivorous and microphagous. Zooplank- ton is captured by feeding polyps. Some have observed the flapping of the tentacles to create a current. Life cycle: In this species, reproduction occurs only in hydroid stage. In this species, there is no free jellyfish stage. The medusae buds carried by the gonozooids never come off. They release directly small ciliated larvae (planula) that will settle and form a new colony. Predators: Some nudibranchs of the genera Eubranchus, Doto, Cuthona and Tergipes are the known predators of this species. Associated species: The nudibranch Doto koenneckeri is specifically associated with this hydroid. Envenomation: This species has a sting which may cause swelling of the affected area in humans (Anon. https://en.wikipedia.org/wiki/Aglaophenia_pluma). 36 3 Biology and Ecology of the Venomous Marine Hydrozoans (Class Hydrozoa)

Gymnangium allmani (Marktanner-Turneretscher, 1890) ( ¼ Gymnangium longicaudatum)

Image credit: Charlotte Richardson. Common name (s): Feather hydroid, burning bush Global distribution: Northern part of the tropical western Atlantic; Brazil, Carib- bean coast of Panama, Puerto Rico and Culebra Is., St. Thomas, Virgin Islands, Martinique. Ecology: It is a coastal species. Biology Description: Stems of this species are up to 9 cm high and are arising from branched, rhizoid stolon. Stem above basal part is with internodes provided with two alternate, closely spaced, short apophyses supporting cladia and three nematothecae: one at base of apophysis and the remaining two are on the anterior and posterior sides of the axil made by the apophysis with the stem internode. Gonothecae are crowded together and are alternately placed along the middle portion of the stem. Gonotheca is borne on short, inconspicuous pedicel. It is barrel shaped, slightly widening distally, rounded basally and is slightly compressed laterally. Envenomation: The toxic element of this species is a venom injected by nematocysts (stinging cells) which ﬁre a venom-ﬁlled harpoon upon contact with a careless human (Nellis 1997). This venomous species has been reported to cause stings every year in Guadeloupe, a region of France in the Caribbean (Rondan 2018). 3.3 Family Aglaopheniidae 37

Macrorhynchia philippina Kirchenpauer, 1872 ( ¼ Lytocarpus philippinus)

Image credit: Danièle Heitz Common name (s): Stinging bush hydroid, white stinger, white smoky-feathered hydroid, fire weed or “fire fern” Global distribution: It is distributed throughout the tropical and subtropical Pacific Ocean, the Indian Ocean, the Atlantic Ocean and the Mediterranean Sea. Ecology: This colonial species is found on artificial substrates (shipwreck and associated ropes); with crevices and outcrops, colonized by corals (Gerardia sp., Stichopathes sp. and Anthipatella wollastoni). This species has also been reported in natural seabeds, such as maërl seabed with the alga Lophocladia trichoclados, sea-barren bottoms dominated by the sea urchin Diadema africanum and edges of Cymodocea nodosa meadows. Depth range is 1–20 m. Biology Description: Colony of this species is irregularly branched and is reaching 4.5 cm in height. Primary tubes of stem and lateral branches are segmented only in the distal region by indistinct oblique nodes. On the stem, just below the hinge joint there is a nematotheca with one opening followed by several nematothecae with two openings; and in the lateral branches, the portion below the hinge joint bears several nematothecae with two openings. Hydrocladia are alternately arranged on the anterior surface of primary tubes. Hydrothecae are elongated, delicate and perisarc thin. Colour of the hydrocauli and branches is very dark in live specimens; and hydrocladia vary from transparent to refringent white. Food and feeding: It feeds mainly on zooplankton. Associated life: The infaunal community of this species (from mäerl seabeds) is composed by sipunculids, sea urchins and crustaceans (schrimps and crabs), together with a dominant goby (Vanneaugobius canariensis). Envenomation: This species is a highly stinger (Anon. http://www.cmas.org/ news/watch-out-for-the-gelatinous-organisms-of-the-eastern-mediterranean). It has 38 3 Biology and Ecology of the Venomous Marine Hydrozoans (Class Hydrozoa) a harmful toxin (Anon. https://www.reeflex.net/tiere/6503_Macrorhynchia_ philippina.htm). Affected people generally develop raised, red, itchy, painful weals; and sometimes blisters form in human skin (Rifkin et al. 1993).

Macrorhynchia phoenicea (Busk, 1852) ( ¼ Lytocarpus phoniceus) Image not available Common name (s): Brown stinging hydroid Global distribution: Tropical Indo-Paciﬁc: New Caledonia, Fiji and Pitcairn; Japan and Australia. Ecology: This reef-associated species is found in sheltered places near the coast and in sublittoral areas. Biology Description: This species is recognized by its bristly appearance, fan-shaped colony and brown colour. Colonies of this species are thin, delicate, reaching 8.5 cm in height. They are branched, multi-pinnate, polysiphonic in the basal part and is composed by a primary tube and several auxiliary tubes. Side branches are in one plane, originating from auxiliary tubes only, bearing alternate hydrocladia. Proximal portions of the stem and branches are bearing median nematothecae only, and the remaining portions are bearing alternate apophyses. Each apophysis supports a hydrocladium associated with two nematothecae and a mamelon on the anterior surface. Envenomation: It is a venomous species (Blaxter et al. 1984).

Monoserius pennarius (Linnaeus, 1758) ( ¼ Lytocarpus pennarius; Macrorhynchia pennarius) Image not available Common name (s): Not designated Global distribution: central and western Paciﬁc and the Indian Ocean; Andaman Islands, Korea strait, South Japan, China Sea, Formosa; Philippines; Singapore; Indonesia; Hawaii. Ecology: It is a shallow-water species occurring at depths of 9–12 m. Biology Description: Colony of this species is 56 cm long, with a large basal mass of matted rhizoids. Hydroclades spring alternately from the anterior tube of the fascicle, and sometimes reach a length of 18 mm. Margin of hydrotheca bears a prominent anterior tooth, and about four indeﬁnite sinuations on each side. Branches bear phylactocarps with sometimes as many as 14 nematoclades. Gonangia spring from near the bases of the nematoclades and are broadly ovate. Envenomation: It is a venomous species (Blaxter et al. 1984). 3.4 Family Apolemiidae 39

3.4 Family Apolemiidae

Apolemia uvaria (Lesueur, 1815)

Image courtesy: Drew Harvell Common name (s): String jellyfish, barbed wire jellyfish, long stringy stingy thingy. Global distribution: Subtropical Atlantic and Pacific Oceans: Norway, USA and Canada. Ecology: This pelagic species can be found from the surface and down to approximately 100 m depth. Biology Description: This species has been listed only in its medusoid stage. Colony may form 30 m long and includes both sexes. Each individual has specific tasks. Some 40 3 Biology and Ecology of the Venomous Marine Hydrozoans (Class Hydrozoa) gather nutrition for the colony, some help with the reproduction while others help in propulsion. Nectophores which is 15–20 mm in size is separated from each other by a cluster of four to six short nectosomal tentacles. Pneumatophore of the colony is bulb-shaped, widest near its apex and is often flecked maroon. Food and feeding: These ocean predators act like drift nets, spreading their tentacles to catch plankton. Envenomation: The tentacles of this venomous species give a painful sting and are to be voided (Anon. https://en.wikipedia.org/wiki/Apolemia_uvaria). Environmental role: Its strong poison may kill large fishes. Skin contact with this species can be very unpleasant. During fall of 1997 an extraordinary swarming of this species created serious trouble for the fish cultivation industry along the Norwegian coast, and considerable amounts of cultivated salmon died (Anon. http://www.seawater.no/fauna/cnidaria/uvaria.html).

3.5 Family Corynidae

Sarsia tubulosa (M. Sars, 1835)

Common name (s): Clapper hydromedusa Global distribution: North Atlantic Ocean including Arctic waters; North Paciﬁc Ocean Ecology: It is abundant in more sheltered coastal waters. Its behaviour during the day consists of periods of swimming by means of series of bell contractions and longer periods of ﬂoating motionlessly, often with greatly extended tentacles and manubrium. Biology 3.6 Family Cuninidae 41

Description: It is a colonial hydroid and a sexual medusa stage. Umbrella of this species is 18 mm high and is somewhat higher than wide. It is bell-shaped, with moderately thick jelly, and a distinct apical chamber of varying shape, usually globular. Its four radial canals pass through the mesogloea to enter the marginal bulbs. Manubrium is very long (about 2.5 times the bell height), tubular and is extending far beyond the umbrella margin. Mouth is circular and simple. Gonads are continuous. There are four equally developed very long tentacles. Marginal tentacle bulbs are broad, with black or crimson ocelli on the abaxial side of the bulbs. Exumbrella is without rows of nematocysts. Statocysts are absent. Individuals are brown, scarlet or blue. Manubrium is pinkish and tentacles and radial canals are pale pink. Envenomation: It is a venomous species (Blaxter et al. 1984).

3.6 Family Cuninidae

Solmissus incisa Image not available Common name (s): Not designated Global distribution: Western coasts of British Isles Ecology: It is a very deep-water oceanic species. Biology Description: Upper portion of umbrella of this species is flat and disk-like. Jelly is fairly thick, but it is very soft and fragile. Lower marginal portion of the umbrella is thin and flexible with 20–40 marginal lappets which are as long as wide. Stomach is large and circular with 20–40 marginal poches which are slightly wider than long. There are 20–40 stiff, tapering marginal tentacles which are slightly longer than the diameter of umbrella. There are two to five marginal sense organs on each marginal lappet. Umbrella of these colourless animals has a diameter up to 10 cm. Food and feeding: These animals use their tentacles for the capture of large, comparatively fast-moving prey. Stomach contents revealed the maximum amount (88%) of gelatinous animals like ctenophores, cnidarians and salps. Its other food items are chaetognaths and euphausiids. Envenomation: This venomous species has haemolytic activity (breaking down of red blood cells—erythrocytes, causing anaemia if there is no compensation from the bone marrow) (Mariottini 2014). 42 3 Biology and Ecology of the Venomous Marine Hydrozoans (Class Hydrozoa)

3.7 Family Eirenidae

Neotima lucullana (Delle Chiaje, 1823) ( ¼ Tima lucellana)

Image credit: Gary L. Hodges Common name (s): Cigar jellyfish Global distribution: North Atlantic Ocean, North Sea and Mediterranean (especially Adriatic and north-west basin). Ecology: It is a member of zooplankton leading a pelagic life. Biology Description: It is a very small, transparent jellyfish with 40–60 marginal white, long tentacles. Its bell width is 68 mm and height is 35 mm. There are seven marginal warts between each pair of tentacles. Its gonads extend along the entire lengths of the radial canals. Envenomation: This species is presumed to be a stinging one (Anon. https:// www.timesofmalta.com/articles/view/20130912/local/two-new-jellyfish-species- recorded-in-maltese-waters.485855). 3.8 Family Geryoniidae 43

3.8 Family Geryoniidae

Liriope teraphylla (Chamisso & Eysenhardt, 1821)

Image Courtesy: Schuchert, Peter, WoRMS Common name (s): Jewel jellyfish Global distribution: Tropical, cosmopolitan species; North Atlantic Ocean, Med- iterranean Sea; east and west South Atlantic and Indo-Pacific Oceans. Ecology: This pelagic, brackish water species is found in inshore, reef and lagoon areas at depths of 3–10 m. It floats normally in great shoals usually near the surface. Biology Description: In this species polyp stage is absent. This species is listed only in medusoid stage. Umbrella is 10–30 mm wide. Umbrella is almost hemispherical. Jelly is thick, especially in apical region. Marginal nematocyst ring is present, with four perradial and four interradial short nematocyst tracks on exumbrella. Velum is well developed. There are four straight radial canals. Manubrium is present on long gastric peduncle of one to three times umbrella height. Mouth is with four simple or slightly crenulated lips. Subumbrellar portion of radial canals is with four, flattened and leaf-shaped gonads which are very variable in shape and size. Envenomation: Nematocysts of this species can be irritating causing dermatitis in humans (Anon. https://www.sealifebase.ca/summary/Liriope-tetraphylla.html). 44 3 Biology and Ecology of the Venomous Marine Hydrozoans (Class Hydrozoa)

Multiple stages of this species caused paraesthesias (burning or prickling sensation) leading to chaﬁng and excoriations in swimmers along the Southern Uruguayan and Northern Argentinean Atlantic coasts. These episodes appear seasonally in the summer and affect groups of bathers in shallow water (1–3 m) (Mianzan et al. 2000).

3.9 Family Haleciidae

Halecium beanii (Johnston, 1838) (¼ Halecium beani)

Image courtesy: Wikimedia Commons Common name (s): Stinging hydroid Global distribution: It is a cosmopolitan species recorded from all oceans, penetrating well into the Arctic Ocean and the subantarctic, but not into the Antarc- tic. In the Atlantic, it occurs as far south as the coasts of Patagonia; it is commonly distributed along the European coasts too. Ecology: The species has been found epizootic on other colonial hydroid, Nemertesia antennina; depth range is 35–180 m. Biology 3.9 Family Haleciidae 45

Description: Colonies of this species are well developed and are composed of a hydrorhiza with numerous tubes from which arise erect hydrocauli. Hydrocladia are partly ﬂexuous, and some of them are larger and slightly branched. Nodes of stem and branches are transverse or slightly oblique. Hydrotheca is placed at upper part of internode. Hydrothecae are shallow and sessile. Envenomation: The stings of this venomous species lead to a rapid urticarial reaction (red and sometimes itchy bumps on the skin) in the affected persons (Burnett et al. 1996).

Nemalecium lighti (Hargitt, 1924)

Common name (s): Not designated Global distribution: Tropical and subtropical Western Central Atlantic: Belize and Bermuda Ecology: This pelagic, brackish water species is also found in mangroves, tidal inlets and sounds. Biology Description: These are small upright colonies (0.5–5 cm), with a generally simple or slightly branched hydrocaule (stem). Extremely branched and dense colonies can rarely be found. Each colony grows from a network of hydrorhizes (stolons) crawling on the substrate. It is protected by a chitinous external skeleton: the perisarc. Hydrocell is covered, especially at the base, with an agglomeration of small debris (suspended matter, algae, diatoms) stuck to the perisarc. Polyps arise from the hydrocolla in two opposite and alternate rows. 46 3 Biology and Ecology of the Venomous Marine Hydrozoans (Class Hydrozoa)

Food and feeding: It feeds on diatoms, eggs and larvae of planktonic invertebrates (bivalves, copepods), and any organic particles in suspension. Predators: These colonies may be prey to small ostracods and pycnogonids in the juvenile stage. Life cycle: Depending on the locality, there are monosexual or bisexual colonies (with both male and female reproductive or gonadal polyps). Reproductive polyps develop directly on hydrorhizes or on hydrocell and are protected by an envelope (gonotheca) in the form of urns, attached by the base. They emit very rudimentary jellyfish or short-lived planktonic jellyfish, which quickly release their sexual products into the environment. The fertilization takes place in open water and the resulting eggs give small mobile planula larvae which will be able to settle and give birth to a new colony. Envenomation: Contacts with this venomous species produced erythematous and highly pruriginous papules in the exposed areas of the body. The signs and symptoms persisted for a week. Pruritus and skin efflorescences however disappeared within a week, leaving no ill effects (Marques et al. 2002; Suput 2011; Barceloux 2008).

3.10 Family Hydractiniidae

Hydractinia symbiolongicarpus (Buss and Yund, 1989)

Common name (s): Not designated Global distribution: It is native to the coastal waters of the north-eastern Atlantic Ocean. Ecology: It lives in shallow environments and is primarily found on hermit crab shells. Biology 3.10 Family Hydractiniidae 47

Description: This species consists of a network of gastrovascular canals embedded in a plate of tissue called the mat. When gastrovascular canals extend outside of the mat, they are called stolons. Colonies exhibit polymorphism that ranges from highly stoloniferous to completely stolonless. Four types of polyps are found on the colonies, including feeding polyps, sexual polyps and two other types of polyps called dactylozooids and tentaculozooids, which protect the colony. While hydractinia species do not have a bodily axis of symmetry, the polyps exhibit oral/ aboral symmetry. In the planula stage, this species exhibits anterior/posterior symmetry. Food and feeding: It feeds on smaller invertebrates found in the shallow mud. Life cycle: Colonies of this species are either male or female, and sexes are probably genetically determined. In the shallow waters, colonies release gametes on a light cue. After a period of darkness, sunlight triggers the rupture of gonadal walls in males and females, causing the release of gametes. Embryos develop in 2–3 days leading to a planula larvae. The planula then attaches to a hermit crab shell and subsequently undergoes metamorphosis to turn into a single polyp with extending stolons. After metamorphosis, the single polyp grows and extends its stolonal network and can reach adult size fairly quickly. The animal can complete its whole life cycle in 2–3 months. Envenomation: Columbus-Shenkar et al. (http://wolfson.huji.ac.il/puriﬁcation/ PDF/Publications/ColumbusShenkar2017.pdf) reported on the isolation of NvePTx1 toxin from this species. Jouiaei et al. (2015a, b) reported that its CfTX-1/2 toxins caused cardiovascular collapse within 1 min in anesthetized rats exposed in vivo to the venom, whereas its CfTX-A/B toxins were more potent with in vitro haemolytic activity. 48 3 Biology and Ecology of the Venomous Marine Hydrozoans (Class Hydrozoa)

3.11 Family Milleporidae

Millepora alcicornis Linnaeus, 1758

Image courtesy: Nick Hobgood, Wikipedia Common name (s): Sea ginger Global distribution: Tropical west Atlantic Ocean Ecology: It is found on shallow-water coral reefs. Encrustations of this species can become established on a variety of structures, not only on coral reefs and rocks but also on dead corals and the hulls of wrecked ships. Later development is in the form of plates or blades in habitats with much water movement such as the surf- pounded outer edges of reefs. Biology Description: Morphology of this species is very variable. Most colonies start as encrusting forms and adopt a branching structure as they grow. In calmer waters, such as in deep lagoons or more sheltered parts of the reef, a more upright, leafy or branched structure develops which can grow to 50 cm tall. On vertical surfaces, the encrusting bases are larger with longer perimeters and the density of branching is lower than it is on horizontal surfaces. Cylindrical branches usually grow in a single 3.11 Family Milleporidae 49 plane and span a range of hues from brown to pale, cream-like yellow, while branch tips are white. Food and feeding: It feeds on plankton and derives part of its energy requirements from microalgae found within its tissues. Life cycle: Reproduction is by either asexual or sexual means. Fragments of the colonies grow into new colonies. This fragmentation is probably the most frequent method of reproduction. Alternatively, certain pores called ampullae contain polyps that bud off short-lived, jellyﬁsh-like medusae, which separate from the colony. They produce gametes which, after fertilization, develop into planula larvae. These drift with the currents as part of the zooplankton before settling out and developing into new colonies. Envenomation: This venomous species can cause painful stings to unwary divers. The cnidocytes of this species are powerful enough to sting human skin. They can inject a venom that causes a painful burning sensation, skin eruptions, blisters and scarring. The toxin of this species was found to be lethal to mice weighing 20 g at 40 μg (Anon. https://en.wikipedia.org/wiki/Millepora_alcicornis). Hernández-Matehuala et al. (2015) reported that the aqueous extract of this species showed haemolytic activity and was lethal to mice (LD50 ¼ 17 μg protein/g) with damage to kidney, liver and lung.

Millepora complanata Lamarck, 1816

Common name (s): Blade ﬁre coral, Mexican ﬁre coral. Global distribution: It is common in Caribbean Sea; Mexico. Ecology: This coral reef-associated species is found in shallow waters with a depth range of 0–15 m. It often grows in areas with vigorous water movement and turbid waters and is tolerant of siltation. Biology 50 3 Biology and Ecology of the Venomous Marine Hydrozoans (Class Hydrozoa)

Description: These colonial coral-like organisms secrete calcareous skeletons. Colonies of this species have an encrusting base and thin upright plates or blades growing to a height of about 50 cm. Surface of the blades is smooth and the outer margins are irregular, with many stumpy protrusions. It is pale brown or cream coloured, with white tips to the blades. Feeding and defensive polyps are hair-like and project through fine pores on the surface of the blades. Food and feeding: Copepods form the main part of the diet of this species. The soft tissues of this species contain zooxanthellae, symbiotic photosynthetic dinoflagellates. These provide much of the organic carbon needed by this species. Life cycle: The reproduction of this species is complex and involves an alternation of asexual and sexual generations. The encrusting parts of the coral expand by the growth of stolons, and the edges of blades expand by sympodial growth. Sexual reproduction involves a sessile polyploid stage and the budding off of planktonic medusae. Envenomation: Contact with this fire coral by bare skin can cause a severe stinging sensation (Anon. https://en.wikipedia.org/wiki/Millepora_complanata). Nematocysts of this species can puncture the human skin and cause painful stings. The crude extract of this species exhibited vasoconstrictor, phospholipase A2 (PLA2) and haemolytic activities in rat erythrocytes (Ibarra-Alvarado et al. 2007). García-Arredondo et al. (2014) reported that contact with this species usually provoked burning pain, erythema and urticariform lesions.

Millepora dichotoma Forsskål, 1775

Image courtesy: Wikimedia Commons Common name (s): Net ﬁre coral 3.11 Family Milleporidae 51

Global distribution: It is found from the Red Sea to Samoa and South Africa Ecology: This species is most abundant in shallow reef habitat at depths of less than 15 m. Biology Description: This species forms fan-shaped colonies up to 60 cm across, but clumps may be several metres across. Coloured mustard to olive yellow, the fans form in a single plane. Corallum of this species is consisting of upright reticulate plates formed by anastomosing ﬂattened branches. Branches in the lower parts frequently unite into solid plates. In the northern Red Sea, this species exhibits four main morphotypes: encrusting, delicate lace-like, leaf-like blades and robust “box-work”. It is suggested that the encrusting morph is always the initial mode of growth in this species and may occur at all depths. Later it is followed by upward growth or “apical shooting” which is usually followed by dichotomous branching and the formation of a lace-like structure. Food and feeding: It feeds on plankton. Envenomation: The stinging nematocysts of this species contain a toxin which causes painful burn-like wounds on contact. At worst, this may cause collapse in those with a severe allergic reaction. Skin irritation may continue for up to 2 weeks (https://en.wikipedia.org/wiki/Millepora_dichotoma; Anon. http://reefkeeping.com/ issues/2002-11/eb/). Crude extracts of this species are highly toxic and displayed haemolytic activity in mice (Ibarra-Alvarado et al. 2007). Hernández-Matehuala et al. (2015) and Radwan (2002) reported that the venom (MCTx-1) of this species was lethal to mice and it showed haemolytic, dermonecrotic, vasopermeable and antigenic properties. Paramasivam et al. (2013) reported that this species exhibited unusual tissue lesions in the form of white spots upon contact. 52 3 Biology and Ecology of the Venomous Marine Hydrozoans (Class Hydrozoa)

Millepora platyphylla Hemprich & Ehrenberg, 1834

Image courtesy: University of California Common name (s): Blade fire coral, plate fire coral, Wello fire coral Global distribution: Indo-Pacific: from the Red Sea and East Africa to northern Australia and French Polynesia. Ecology: It is a coral reef-associated species. Biology Description: This species forms large colonies. These are commonly 200–300 cm in diameter and are composed of anastomosed vertical plates, which may reach 200 cm in height. Envenomation: The nematocyst venoms (Mp-TX) of this species displayed haemolytic, vasopermeable and dermonecrotic properties (Ibarra-Alvarado et al. 2007; Hernández-Matehuala et al. 2015; Radwan 2002). 3.11 Family Milleporidae 53

Millepora tenera Boschma, 1949

Image courtesy: ReefLifeApps, WoRMS ?Please inform the author before republishing. Author ReefLifeApps.com Common name (s): Stinging coral Global distribution: Western Indo-Pacific: from the Red Sea and the eastern coast of Africa to Japan, Australia, American Samoa and the Mariana Islands. Ecology: It is found at depths of 0–40 m; often in turbid locations where it is tolerant of some degree of siltation. Biology Description: Branchlets of this species are fan-shaped. Corallum is forming a hemispherical cluster of fan-shaped branches radiating from a central point. Branches are flattened. Surface is very fine and smooth. Pores are difficult to notice because of the fine surface structure. Food and feeding: This species gains its nutrients via their special symbiotic relationship with algae known as zooxanthellae which live inside the tissues of this coral. Envenomation: The nematocysts’ venoms of this species showed lethal effects in mice (Ibarra-Alvarado et al. 2007). This species causes painful rashes when it is touched by bare skin. Extracts of this coral have been reported to contain neurotoxins which can cause convulsions, respiratory failure and death in mice. Further, the extract causes haemolysis, contains a dermonecrotic factor and has antigenic properties (Anon. https://en.wikipedia.org/ wiki/Millepora_tenera; Wittle et al. 1974). 54 3 Biology and Ecology of the Venomous Marine Hydrozoans (Class Hydrozoa)

Millepora sp. Envenomation: This unidentiﬁed species caused skin irritation upon contact. It is suggested that the high levels of phospholipases A2 (PLA2) activity in its venom may be responsible for this effect (Suput 2011).

3.12 Family Olindiidae

Gonionemus vertens A. Agassiz, 1862 ( ¼ Gonionemus oschoro)

Image courtesy: Flickr, creative commons Common name (s): Clinging jellyfish, orange-striped jellyfish, angled hydromedusa Global distribution: Circumglobal in northern temperate coastal waters; Pacific coast: from The Aleutian Islands to Southern California; Atlantic coast: from Massachusetts to New Jersey; Asia: northern Zhejiang, the Sea of Japan, Olga Bay and northern Japanese Islands; Europe: from Mediterranean Sea to Norway and Swedish west coast. Ecology: It is found attached to kelp, eelgrass and other substrates; brackish coastal waters. Biology Description: This bell-shaped hydromedusa (usually just slightly broader than tall) has about 60–80 unbranched tentacles. Umbrella is 2.5 cm wide. Tentacles have large rings of nematocysts all along their length and partway back from the tip of each tentacle is a larger adhesive knob or pad. Tentacle tends to bend at the disk. Tentacle bulbs at the base of the tentacles are yellowish-tan. There are four radial canals which are unbranched and are continuing all the way to the margin of the bell. Orange, red, violet (in females), or yellow-brown (in males) gonads hang down along the four radial canals and form a clearly visible X shape. Manubrium is 3.12 Family Olindiidae 55 coloured tan and hangs down about to the bell margin, with four slightly frilly lips. Bell may be clear or light green. Food and feeding: It feeds on small crustaceans, especially copepods. Envenomation: Polyp which is seldom seen in this species is highly venomous (Anon. https://inverts.wallawalla.edu/Cnidaria/Class-Hydrozoa/Hydromedusae/ Gonionemus_vertens.html). This venomous species has been reported to have increasing numbers of stinging incidents occurring on the US Atlantic coast and its sting severity is medium (Anon. https://en.wikipedia.org/wiki/Gonionemus_vertens; Montgomery et al. 2016; Williamson et al., 1996). Pigulevsky and Michaleff (1969) have reported that this species has been implicated in numerous cases of injuries to humans bathing in the Sea of Japan. The venom of this species not only produced pain and other local manifestations but also caused neuropsychiatric changes. Of 500 persons stung by G. vertens during the past year in the Far East, 99 were observed to have polyneuritis, polyradiculitis and arthralgia, as well as visceral reactions. Psychiatric aberrations were seen as the only manifestation of envenomation in 30 patients, and in combination with neurologic symptoms in 371.

Olindias formosus (Goto, 1903) ( ¼ Olindiodes formosa)

Image courtesy: Wikipedia Common name (s): Flower hat jelly 56 3 Biology and Ecology of the Venomous Marine Hydrozoans (Class Hydrozoa)

Global distribution: North-western Pacific off central and southern Japan, and South Korea’s Jeju Island Ecology: During the day, this species rests on the bottom, often among rocks or algae, but at night it floats up to hunt for their prey, typically small fish. Biology Description: Both polyp and medusoid stages have been recorded in this species. Polyps form small colonies that are stolonal, occurring in small clusters. Hydrorhizae are cylindrical with small egg-shaped or cylindrical hydranths (200–800 mm length) occurring along a relatively straight stolon up to 5 mm in length. Each hydranth has a single, elongate, filiform tentacle and is transparent or whitish in colour. Its single tentacles are very active, showing almost constant sweeping motions. Medusa of this fluorescent jelly has brilliant, multicoloured tentacles that coil and adhere to its rim when not in use. Its bell is translucent and pinstriped with opaque bands. This jelly can grow to a size of about 15 cm in diameter. Life cycle: The hydroids of this species are found attached themselves to various surfaces and formed small clusters. These hydroids release the medusae which have a diameter of about 1 mm. Envenomation: The sting of this venomous jelly is painful, leaving a bright rash (Williamson et al. 1996; Anon. https://www.montereybayaquarium.org/animal- guide/invertebrates/flower-hat-jelly). In Japan this species has caused severe envenoming associated with human fatality (Wikipedia; Anon. https://www. vapaguide.info/catalogue/NORAM-CNI-147).

Olindias muelleri Haeckel, 1879 (¼ Olindias phosphorica)

Image courtesy: Fred Hsu; Wikipedia 3.12 Family Olindiidae 57

Common name (s): Cigar jellyfish Global distribution: This subtropical species has a broad global distribution and is known from temperate Atlantic waters and from the Mediterranean. Ecology: It is a pelagic species leading a planktonic life. Biology Description: Umbrella of this species is armed with a battery of relatively short, blue tentacles. Its radial canals are arranged in a distinctive red cross-like pattern. There are 11–19 centripetal canals per quadrant; 30–60 primary tentacles; 100–120 secondary tentacles and 100–170 marginal clubs. Diameter of umbrella can reach 8 cm. It is transparent in colour with four radial gonads. Food and feeding: These animals basically eat plankton. Life cycle: This species has both medusa and polyp phases in its life cycle. In the sexual reproduction, a zygote becomes a planula larva that settles at the bottom of the sea and forms a polyp which gives rise to juvenile medusa through asexual reproduction. Envenomation: This species has been reported to inflict only a very mild sting which is not perceived by the majority of bathers (Montgomery et al. 2016; Anon. http://oceania.research.um.edu.mt/jellyfish/cards/G.html). Anon. (http://www.cmas.org/news/watch-out-for-the-gelatinous-organisms-of- the-eastern-mediterranean) however reported that this jelly fish is a serious stinger in Central and East Atlantic, and the Mediterranean Sea. Marsh and Slack-Smith (2010) reported that its mild or sharp sting may last for 30 min associated with the formation of faint pink weals (red, swollen marks left on flesh) which may last for about 2 h.

Olindias sambaquiensis Muller, 1861

Common name (s): Not designated 58 3 Biology and Ecology of the Venomous Marine Hydrozoans (Class Hydrozoa)

Global distribution: It is endemic to the tropical, Southern Atlantic, with distribution between the south-east region of Brazil and the north of Argentina Ecology: It is a pelagic, planktonic species. Biology Description: Max length: 10.0 cm, 21–27 centripetal canals per quadrant; 80–100 primary tentacles; 200–300 secondary tentacles; 100–200 marginal clubs; 50–100 mm wide. Envenomation: This venomous species has been known to cause severe envenoming in Japan in the south-western Atlantic ocean, along the coasts of Brazil, Uruguay and Argentina (Williamson et al. 1996; Anon. https://www.vapaguide.info/ catalogue/NORAM-CNI-147). Resgalla et al. (2011) reported that this species caused injuries of moderate severity in the victims associated with 3300 accidents of south-east and south regions of Brazil. These victims had skin irritations with lesions and marks. Haddad et al. (2014) reported on the occurrence of two cytolytic peptides viz. oshem 1 and oshem 2 in this species and these cytolysins showed haemolytic activity. Pereira et al. (2018) reported on the human envenomation of this species. The victims developed systemic reactions associated with intense muscular pain, cardiac arrhythmias, low cardiac output and shock. Children (due to the greater compromised body area) were the most affected. Haddad et al. (2002) reported on 29 accidents caused by this species in the south- eastern coast of Brazil. The victims developed mild pain, round plaques and no systemic symptoms.

Olindias singularis Browne, 1905 Image not available Common name (s): Not designated Global distribution: Tropical Indo-West Paciﬁc: Maldives, Chagos, India, Australia and Philippines Ecology: This is a pelagic, planktonic species. Biology Description: Bell of this species is circular and saucer-like with a maximum diameter of 3.5 cm. There are 30–80 primary tentacles hanging from the bell rim. There are also secondary tentacles (15–50) which are longer than the primary ones. There are 4–12 centripetal canals in each quadrant and a single statocyst is situated at the origin of each primary tentacle. Gonads are present on the radial canals. Envenomation: This venomous species gives a mild or sharp sting which lasts about 30 min. Faint pink weals form after 15 min and last for about 2 h (Williamson et al. 1996; Marsh and Slack-Smith 2010). 3.13 Family Pandeidae 59

3.13 Family Pandeidae

Leukartiara gardineri Browne, 1916

Image Courtesy: WoRMS Common name (s): Little red stinger Global distribution: Central North Paciﬁc; Western Australia and Queensland Ecology: This planktonic species occurs between 150 m depth and the surface. Biology Description: It is a small hydromedusa and its conical bell is only 10 mm high by 5 mm across. Bell which is clear at the apex is ﬁlled with its orange gonads and the large, red, folded mouth. Four, 25 mm long pink tentacles and numerous minute tentacles hang from the edge of the bell. It is possessing small interradial and adradial tentaculae between the four perradial tentacles. Manubrium extends to near the velar level with a clear constriction near its mouth. Cord-like exumbrellar spurs extend from the tentacle bulbs to near the apex of the bell. 60 3 Biology and Ecology of the Venomous Marine Hydrozoans (Class Hydrozoa)

Envenomation: Marsh and Slack-Smith (2010) and Burnett et al. (1996) reported that it is relatively a harmless stinger, producing a very sharp sting pain which subsides rapidly leaving no local effects. Blaxter et al. (1984) reported that it is venomous species and its venomology is little known.

Pandea conica (Quoy & Gaimard, 1827)

Common name (s): Conical medusa Global distribution: Tropical south-west Atlantic and the Mediterranean: Italy, Brazil and Spain; North-East Atlantic, North Sea and English Channel Ecology: It is a planktonic species living near water surface. Biology Description: It is a small hydromedusa reaching 3–4 cm. Umbrella of this species is bell-shaped. A yellow-orange border line runs around the umbrella. There are 16–44 marginal tentacles with conical, laterally compressed bulbs. Stomach is with a broad base; it is about half height of umbrella and is with four simple lips. There are four perradial canals with smooth edges. Ring canal is moderately broad. Gonads lie on entire interradial walls of manubrium, forming coarse-meshed network of ridges with pits in between. Colour of stomach and tentacle bulbs is ochre-brown. 3.13 Family Pandeidae 61

Envenomation: It is a mild stinging species (Anon. http://lifecubomed.es/media/ cms_page_media/1/Cubomed%20guide_2014.pdf)-length up to 6 cm.

Pandea rubra Bigelow, 1913

Image credit: VlaPickles. Wikipedia Common name (s): Red paper lantern jellyﬁsh Global distribution: It has been reported from boreal to sub-boreal waters in the North Paciﬁc and North Atlantic, and also in the Southern Ocean in Japan Ecology: These animals are found in extremely deep waters at depths between 450 and 1000 m. Biology Description: This medusa has a transparent, bell-shaped hood measuring about 10 cm in diameter and 17 cm from top to bottom. It has 14–30 tentacles that extend up to six times the length of its body. Inside the transparent hood is a deep-red- coloured mantle. Manubrium is broad. Mouth rim is cruciform with strongly folded and crenulated lips. Gonads lie on entire interradial areas, forming very close- meshed irregular and complex network of ridges with pits in between subumbrella, manubrium, velum and tentacles are with deep brownish-red colouration. This species exhibits bioluminescence. Envenomation: Crude extracts of this venomous species showed haemolytic activity (Kawabata et al. 2013; Mariottini 2014). 62 3 Biology and Ecology of the Venomous Marine Hydrozoans (Class Hydrozoa)

3.14 Family Pennariidae

Pennaria disticha Goldfuss, 1820 ( ¼Pennaria tiarella)

Image credit: Larry Basch, Wikipedia Common name (s): Feather hydroid, Christmas tree hydroid Global distribution: Tropical and subtropical Indo-Pacific, Atlantic Ocean, Carib- bean and the Mediterranean. Ecology: This shallow water (0–29 m), sessile species is found attached to artificial and natural hard substrates where there is some water movement. It is very common as fouling in harbours throughout the main islands and is commonly found on reefs usually in more protected areas or in cracks and crevices. It is also found in brackish waters. Biology Description: Feather-like colonies of this species are large; as tall as 30 cm and is with a dark brown to black perisarc, a protein-chitin exoskeleton which surrounds the stem and branches. This perisarc is usually overgrown with diatoms and algae, making the branches of the hydroid appear muddy brown. Branching is alternate. Polyp has a circle of 10–18 filiform tentacles at the base and as many as 12 capitate tentacles on the upper part of the hydranth. Polyps are white with a reddish tinge. Annulations occur on the branches which bear the polyps, and on the main stem and side branches. This species also exhibits a pelagic medusoid stage. Food and feeding: This hydroid is a carnivore. The polyps spread out their tentacles to catch any small zooplankton that float by. The prey is often captured and immobilized by nematocysts on the thread-like tentacles at the base of the polyp. The crown bends over to catch the food item, which is then killed by the more powerful nematocysts at the tip of the crown tentacles and thrust into the mouth. Life cycle: This species exhibits both asexual and sexual reproduction. During asexual reproduction, the medusa (gonophores) bud off singly from the hydranth body just above the proximal tentacles. These medusae generally break away from 3.15 Family Physaliidae 63 the colony and swim about during the discharge of the sex products. At the onset of spawning, the ripe medusae gradually begin a rhythmic twitching. The males emit puffs of white sperm, the females eject three to six eggs. Fertilization is external. In about a day, developing embryo becomes a young free-swimming planula, which will eventually settle and develop into a young hydroid colony. Envenomation: The sting of this species yielded a noticeable pain and discomfort, but it is not lethal (Gibbons et al. 1990). It has been reported that an acute, painful dermatitis occurred in several people who came into contact with a rope on which this species was growing as a fouling organism (Tezcan and Sarp 2013; Anon. https://en.wikipedia.org/wiki/Pennaria_ disticha).

3.15 Family Physaliidae

Physalia physalis (Linnaeus, 1758) (¼ Physalia utriculus)

Image credit: Shutterstock Common name (s): Portuguese man o’ war Global distribution: Warm tropical and subtropical water; Atlantic Ocean, the Pacific Ocean, the Indian Ocean, the Caribbean and the Sargasso Sea Ecology: It is a member of zooplankton floating on or near the surface of the water. Biology Description: Colony of this species is consisting of four types of polyps: a pneumatophore or float; dactylozooids or tentacles; gastrozooids or feeding zooids; and gonozooids which produce gametes for reproduction. Cnidocytes (stinging cells) are present in the tentacles. P. physalis has two sizes of cnidocytes, some small and others are large. These cells retain their potency long after an individual has been washed up along the shore. It floats by the aid of its pneumatophore, or float 64 3 Biology and Ecology of the Venomous Marine Hydrozoans (Class Hydrozoa) which is a long, gas-filled bladder, formed as an overgrown polyp in the shape of a closed bag. Some Men-of-War are “left-sided”, while others are “right-sided”. Left- sided individual drifts at an angle of 45 to the right of the direction from which the wind is blowing, and the right-sided individual does the opposite (Santhanam et al. 2015; Santhanam and Srinivasan 1994). Food and feeding: The Portuguese Man-of-War traps its food items such as fish fry (young fish), small adult fish, shrimp and other small animals in the plankton in its tentacles. Nearly 70–90% of the prey of this species are fish. The food of the Man- of-War is digested in its bag-like stomachs (gastrozooids), which are located along the underside of the float. The gastrozooids digest the prey by secreting enzymes that break down proteins, carbohydrates and fats. Each Man-of-War has multiple gastrozooids complete with individual mouths. After the food has been digested, any undigestible remains are pushed out through the mouths. Predators: The Portuguese Man-of-War is eaten by some fish and crustaceans (e.g. the sand crab). Life cycle: An “individual” of this species is actually a colony of unisexual (dioecious) organisms. Every individual has specific gonozooids (sex organs or reproductive parts of the animals, either male or female). Each gonozooid is comprised of gonophores, which are containing either ovaries or testes. Fertilization of this species occurs in the open water because gametes from the gonozooids are shed into the water. Fertilization may take place close to the surface. Envenomation: This species can hurt tourists and tourism in areas where it is common, due to its stings containing cnidocytes rich in neurotoxin. Much money is spent each year to treat swimmers who have been stung by the tentacles of individuals that have washed up on beaches. The inflammatory response resulting from its stings is due to the release of histamines from mast cells within the victim (https://animaldiversity.org/accounts/Physalia_physalis/). Montgomery et al. (2016) and Frazão and Antunes (2016) reported that the potent haemolysin (glycoprotein venom), viz. physalitoxins P1, P3, and PpV9.4, of this species is responsible for both haemolytic and lethal activities. Mariottini (2014) and Suput (2011) reported that the extracts from this species caused anaphylaxis (acute allergic reaction after a sting) and immunologic complications after contact with this dangerous hydrozoan. Further, death due to cardiovascular collapse and reactive arthritis have also been recorded in patients stung by this species. Tibballs et al. (2011) reported that the stings of these species, which resemble a “string of beads”, cause sharp pain which may extend beyond the site of the immediate lesion. The pain usually subsides quickly and the sting fades within hours to days. Occasionally however the wound may blister and a systemic illness consisting of headache, vomiting, abdominal pain and diarrhoea is provoked. The few deaths following stings in Atlantic waters have been attributed to cardiovascular toxicity. 3.16 Family Porpitidae 65

3.16 Family Porpitidae

Porpita porpita (Linnaeus, 1758) (¼ Porpita paciﬁca)

Image credit: Bruce Moravchik, Wikipedia Common name (s): Blue button jellyfish Global distribution: Warm waters off Europe, in the Gulf of Mexico, Mediterra- nean Sea, New Zealand, and southern USA Ecology: These hydroids live on the ocean surface as passive drifters (zooplankton); sometimes they are blown into shore, and sometimes seen in thousands. Biology Description: Blue button jellies are relatively small and measure about 2.5 cm in diameter. They consist of a hard, golden brown, gas-filled, golden brown float of 2.5 cm wide in the centre and this is surrounded by blue, purple or yellow hydroids which are bright blue turquoise to a yellow colour. Each strand has many branchlets that end in knots of stinging cells called nematocysts (Kennedy 2019; Santhanam et al. 2015; Santhanam and Srinivasan 1994). Food and feeding: Blue button jellies eat zooplankters such as copepods, crustacean larvae and other small organisms. It has a single mouth located beneath the float to eat its prey and get rid of its wastes. Predators: These animals are normally eaten by sea slugs Glaucus atlanticus and violet sea snails. Life cycle: Blue buttons are hermaphrodites, i.e. each blue button jelly has both male and female sex organs. They have reproductive polyps that release eggs and 66 3 Biology and Ecology of the Venomous Marine Hydrozoans (Class Hydrozoa) sperm into the water. The eggs are fertilized and turn into larvae, which then develop into individual polyps. Blue button jellies are actually colonies of different types of polyps; these colonies form when a polyp divides to form new types of polyps. Envenomation: The tentacles of this species have stinging cells called nematocysts and these organs are responsible for mild stinging (Anon. https:// www.thoughtco.com/blue-button-jelly-porpita-porpita-2291819, http:// lifecubomed.es/media/cms_page_media/1/Cubomed%20guide_2014.pdf). Anon. (https://www.thoughtco.com/blue-button-jelly-porpita-porpita-2291819) and Oiso et al. (2005) reported that these jellies do not have a lethal sting, but they can cause skin irritation (dermatitis) in humans when touched. So it is best to avoid these beautiful organisms.

Velella velella (Linnaeus, 1758)

Common name (s): By-the-wind sailor Global distribution: Warmer regions of the Southern and Northern Hemispheres; Atlantic Ocean and Pacific Ocean Ecology: This coastal species is a member of zooplankton and is found floating on the surface of the high seas. Biology Description: It is a highly modified individual hydroid polyp, and not a colonial hydrozoa. It is blueish to purple with a flat oval transparent float and an erect sail projecting vertically at an angle to the axis of its body. Projection of the sail helps the animal to take the best advantage of the wind, at any given moment. Its mouth is located in the middle of the underside of its body and lacks tentacles. Older zoological opinions however classified this species as a siphonophore, along with the Portuguese man-of-war and other colonial creatures. In contrast, recent taxonomists have classified this species as a chondrophore along with two or three uncommon relatives (Santhanam et al. 2015; Santhanam and Srinivasan 1994). Food and feeding: It is a carnivorous hydroid polyp, feeding on small prey and fish that can be caught only immediately below the surface of the water. Predators: Violet sea slug, Hypselodoris violacea. 3.16 Family Porpitidae 67

Life cycle: When biologists looked at the Velella velella as a colonial hydrozoan, the colonies were said to be hermaphroditic and the gonophores dioecious. The reproductive polyps were thought to produce medusa, which would break away from the colony and reproduce sexually, giving rise to planula larva. In recent studies, this species has been recognized as a single hydroid where reproduction still consists of an alternate generation between polyp and medusa stages. The life cycle series of this species include polyp-medusa-egg-planula-polyp. Envenomation: Anon. (http://lifecubomed.es/media/cms_page_media/1/ Cubomed%20guide_2014.pdf) reported that the sting of this species is mild. Although Velella toxins are harmless to humans, it is not a good idea to handle the jelly creatures and then touch your eyes or mouth. The Velella neurotoxin might cause itching (Oskin 2015). 68 3 Biology and Ecology of the Venomous Marine Hydrozoans (Class Hydrozoa)

3.17 Family Rhizophysidae

Rhizophysa eysenhardti Gegenbaur, 1859

Image credit: Lubitz Ilan, Flickr Common name (s): Not designated Global distribution: Tropical and subtropical Eastern Pacific: Mexico, Costa Rica, USA and Canada Ecology: This is an epi- and mesopelagic species found in the water column. It may form swarms. Biology Description: This species has been listed only in its medusoid stage. It is a small planktonic animal measuring 15 cm when extended. There are long internodes between gastrozooids. Each gastrozooid has a single tentacle. When the gastrozooids 3.17 Family Rhizophysidae 69 are mature, it is not entirely obvious that they arose in two separate rows, but the alternate attachment of the tentacle to the left and right sides of the gastrozooids is clearly seen. Median row of siphosomal elements, found between the left and right rows of gastrozooids, consists solely of gonodendra. Gonodendron buds are found just as far to the anterior as the gastrozooid buds are. Food and feeding: It is a predator feeding only on fish larvae. Envenomation: It is capable of inflicting venomous stings in human beings (Cooke and Halstead 1970). Anon.(https://publications.csiro.au/rpr/download?pid¼csiro:EP1312313& dsid¼DS2) reported that the stings of this species, like those of many siphonophores, are painful. They are often encountered by fishermen when handling their lines.

Rhizophysa ﬁliformis (Forsskal, 1775)

Image credit: Riek, Denis, WoRMS Common name (s): Not designated 70 3 Biology and Ecology of the Venomous Marine Hydrozoans (Class Hydrozoa)

Global distribution: Cosmopolitan; subtropical Western Atlantic Ecology: It is a member of zooplankton. Biology Description: This species has been listed only in its medusoid stage. This species has a uniserial development of gastrozooids and gonodendra. There are one to six gonodendra found between the mature gastrozooids. It has a relatively large spherical pneumatocyst (air bladder or ﬂoat) which may be round or oblong, and is typically plum-coloured on top. Colony can relax to several metres or contract to several centimetres. Envenomation: The stings of this species like those of many siphonophores are painful. They are often encountered by ﬁshermen when handling their lines (Anon. https://publications.csiro.au/rpr/download?pid¼csiro:EP1312313&dsid¼DS2).

3.18 Family Rhopalonematidae

Colobonema sericeum Vanhoffen, 1902

Common name (s): Silky medusa, midwater jelly Global distribution: It is a warm and temperate water species occurring in all three oceans except in the Mediterranean. Ecology: It is a deep-sea hydrozoan occurring at depths of about 600 m. Biology Description: Umbrella of this species is up to 45 mm wide, 40 mm high and is slightly conical. Manubrium is short and tubular. There are eight narrow gonads which are linear, along greater part of radial canals. There are 32 short stump-like solid marginal tentacles. Velum is very well developed. Stomach is four-sided of varying length but is not extending beyond umbrella margin. Mouth is with four short simple pointed lips. Whole medusa is colourless; stomach, marginal tentacles and gonads are less transparent and subumbrellar musculature is iridescent. 3.18 Family Rhopalonematidae 71

Envenomation: Extracts from this species have shown haemolytic activity (Mariottini 2014).

Crossota rufobrunnea (Kramp, 1913)

Common name (s): Not designated Global distribution: Boreal Atlantic but not in the Norwegian or polar seas; south- west of Ireland and west of north Scotland Ecology: It is a deep-water species. Biology Description: Umbrella of this species is slightly higher than a hemisphere with or without the trace of apical process. Jelly is moderately thin. Velum is moderately broad. Stomach is short and pyriform without peduncle. Mouth is with four short lips. There are eight broad, straight, ribbon-like radial canals. Ring canal is narrow. Eight sausage-shaped gonads are hanging down into subumbrellar cavity from junctions of radial canals with stomach. There are 200–250 short, solid marginal tentacles. Diameter of umbrella is 10–15 mm. Colour of umbrella, velum, stomach and marginal tentacles are deep reddish brown. Envenomation: Extracts of this species have shown haemolytic activity (Mariottini 2014). 72 3 Biology and Ecology of the Venomous Marine Hydrozoans (Class Hydrozoa)

Pantachogon haeckeli Maas, 1893

Image credit: Russ Hopcroft Common name (s): Not designated Global distribution: Polar, circumglobal Ecology: It is a deep-sea species occurring at depths of 0–1875 m. Biology Description: Umbrella is 12 mm wide and high and is with very strong and conspicuous musculature. There are 64 tentacles and 64 free statocysts. Gonads lie along greater part of eight radial canals. Envenomation: Crude extracts of this species showed haemolytic activity (Kawabata et al. 2013; Mariottini 2014).

3.19 Family Sertulariidae

Sertularia cupressina Linnaeus, 1758 3.19 Family Sertulariidae 73

Image credit: Flickr Common name (s): Sea cypress, sea cypress hydroid, white weed, squirrel’s-tail hydroid Global distribution: Subtropical Atlantic and Arctic Oceans: USA, Canada and Germany Ecology: This reef-associated species is found in a range of habitats from estuaries to the open coast attaching to hard substrata such as scallop shells, characteristically in sandy areas. They are also found on oyster beds at depths of 1–100 m. Biology Description: This colonial hydroid is notable for its white or silvery colour. It largely resembles a plant with both branches and a stem. Colonies are branched, erect, bushy and is up to 50 cm in length. In general, there are only two branches per internode with the upper part of the stem slightly spiralled. Hydrothecae (cup-shaped extensions) alternate and are tubular with two teeth. Small polyps on the branches are able to retract into the bottle-shaped openings of the cups. If a single “feather” is viewed under a microscope, the small pockets that once housed the tiny polyp could be seen fairly clearly. Food and feeding: This species like other hydroids captures plankton suspended in water with the urticant tentacles of the feeding polyps, the gastrozoids. The tentacles are covered with cnidocytes and are arranged concentrically around the mouth. Prey is then directed to the mouth at the top of each polyp. Life cycle: Reproduction occurs only in hydroid stage. It is a gonochoric species and it has separate male and female colonies. Fertilization and early development of the planula take place in the ripe gonophores. The larvae planula is rather demersal and it does not swim on the surface. But it can move for 2 or 3 days or more, then it is fixed on a hard substrate close to his parents. It then metamorphoses into an erect colony. Colonies can be broken, fragmented and torn by fishing gear. This species has a high regeneration capacity by budding during the long fixed phase. The life span of a colony is about 3 years. Envenomation: It is a venomous species (Russell 1965) and its venomology is not known. Biology and Ecology of the Venomous Marine True Jellyfish (Class Scyphozoa) 4

4.1 Family Atollidae

Atolla vanhoeffeni Russell, 1957

Image credit: Fisheries and Oceans Canada Common name (s): Not designated Global distribution: Subtropical Atlantic and Paciﬁc Oceans: Canada, Ireland and USA. Ecology: It is a bathypelagic species. Biology

# Springer Nature Singapore Pte Ltd. 2020 75 R. Santhanam, Biology and Ecology of Venomous Marine Cnidarians, https://doi.org/10.1007/978-981-15-1603-0_4 76 4 Biology and Ecology of the Venomous Marine True Jellyfish (Class Scyphozoa)

Description: This species is occasionally larger with 20 marginal tentacles. Base of stomach in shape of square-sided cross is with right-angled corners and straight sides, and with a total of eight dark pigment spots next to outer corners. Its single “hypertrophied” tentacle is in exactly same radius as septum between lobes of stomach (i.e. opposite an inner corner of stomach-cross). There are no papillae on marginal lappets. Diameter of the animal is up to about 30 mm. It is a bioluminescent species. Envenomation: This stinger has shown haemolytic activity (breaking down of red blood cells—erythrocytes; causing anaemia if there is no compensation from the bone marrow) (Mariottini 2014; Anon. https://www.facebook.com/USPS/posts/ 10156187481249810).

Atolla wyvillei Haeckel, 1880

Image credit: Edith A. Widder, Wikipedia Common name (s): Wyville’s crownjelly Global distribution: Tropical Antarctic, Atlantic and Pacific Oceans: Philippines, Brazil, Canada and USA; Gulf of Mexico and New Zealand. Ecology: It is a deep-water species. In open waters, it occurs in daytime at a depth of 500–1500 m and is closer to the surface at night. Biology Description: It is a bioluminescent species. Umbrella of this species is flattened and disc-like. It measures as little as 1.5 cm across to 20 cm across. Exumbrella is with a deep circular, coronal furrow situated nearer umbrella margin than apex. It has 22 marginal tentacles around the rim of the body and one hypertrophied tentacle, which is 1.5 times to 36 times longer than the bell’s diameter. This tentacle often coils and retracts into the jellyfish’s bell. Base of stomach is in the shape of a four- leaved clover. Manubrium is wide, projecting below disc and is with four leaf- shaped somewhat pointed, perradial lips. Its eight gonads first develop as crescent- shaped endodermal thickenings. In mature females, each gonad is distinct, oval or bean-shaped, and in mature males, the gonads are irregularly folded and lengthened 4.1 Family Atollidae 77 appearing as a more or less continuous circle of gonad tissue. Animal is completely covered with a thin, very delicate, dark reddish brown epithelial layer; and stomach walls are intensely dark. Food and feeding: The hypertrophied (trailing) tentacles of this species passively trap food such as crustaceans and organic matter that float by in ocean currents. Life cycle: It is believed that the tentacles of this species help in sexual reproduction by reaching out in search of potential mates. It can reproduce asexually and sexually. Like many other members of the Scyphozoa class, this species can develop into polyps, asexually producing buds that grow into larvae. Envenomation: The tentacles of this species are one-armed with poisonous bumps named nematocysts which inject poison at the touch (Prezi, https://prezi. com/ekdzrscb1-ku/atolla-wyvillei/). Mariottini (2014) reported that this species has haemolytic activity.

Atorella subglobosa Vanhoffen, 1902 Image not available Common name (s): Not designated Global distribution: Tropical eastern central Atlantic: Canary Island, East coasts of Africa and Malay Archipelago; South Paciﬁc Ocean. Ecology: It is a pelagic species. Biology Description: Bell of this species is 1.5–1.7 cm wide and globular. Exumbrella is smooth. Ring furrow is not very deep. Marginal lappets are shallow and are slightly cleft. There are 20 gastric ﬁlaments in each of the four groups. Stomach is four-sided and six rhopalia are arising from very shallow niches in bell margin. Four to six interradial sac-like, swollen gonads are seen, and tentacles are without terminal knob. Stomach is brown; gonads are yellowish brown; subumbrellar musculature is white and all other parts are translucent. Life cycle: Reproductive strategies of this species are unknown. Envenomation: The sting severity of this venomous species is mild (Montgomery et al. 2016). 78 4 Biology and Ecology of the Venomous Marine True Jellyfish (Class Scyphozoa)

4.2 Family Cassiopeidae

Cassiopea andromeda Forsskal, 1775

Common name (s): Upside-down jellyfish, Persian Gulf jellyfish Global distribution: Tropical Indo-Pacific. Ecology: It usually lives in intertidal sand or mud flats, shallow lagoons, around mangroves and among seagrass beds. Biology Description: It is called “Upside-down jellyfish” because it usually lies mouth upward on the sea bottom. Umbrella of this species is circular, flattened and is 10–15 cm in diameter. Its subumbrellar surface is facing upwards and exumbrella is facing downwards. Oral arms are 8–9 in number and are slightly longer than umbrella radius. They are branched, with about four side branches. Each arm has numerous small and about six large, club-shaped vesicles. These medusae are brown, blue or green; and umbrella is usually brown with white patches on its rim. Food and feeding: It is a carnivorous species and it eats small animals from the sea or just pieces of them after it paralyses its prey with its mucous and nematocysts when they are released. Association: This jellyfish also lives in a symbiotic relationship with photosynthetic dinoflagellate algae, the zooxanthellae. While the jellyfish protects the algae by its nematocyst from fish, in turn, the algae provide food produced by photosynthesis. It is also the host of the amphipod Hyperia galba. Life cycle: This jellyfish like other cnidarians has an asexual and sexual reproduction. It reproduces by budding when it is in a polyp form. When it is in a medusa form, it reproduces sexually. The female medusa produces the eggs and keeps them. As the male produces the sperm and releases them in the water, the female uses its tentacles to bring the sperm to fertilize its eggs. Envenomation: Its sting may result in pain, rash and swelling on contact area. Vomiting and muscle pains may occur depending on victim’s sensitivity to the toxin 4.2 Family Cassiopeidae 79 of nematocysts (Anon. http://www.cmas.org/news/watch-out-for-the-gelatinous- organisms-of-the-eastern-mediterranean; Wikipedia). The crude venom of this species produced pain when applied to human lips, resulted in lethality to mice at a dose of 0.21 mg protein kg/mouse; and 50 μg protein caused vasopermeability and dermonecrosis after injection into mouse skin. Further- more, crude venom of this species was also shown to have phospholipase A2 activity and to induce lysis of mouse lymphocytes. Dosages of 1 μg protein lysed 50% of treated human erythrocytes (Mariottini and Pane 2010). While the sting severity of this venomous species is mild, the venom of this species showed haemolytic activity against human RBCs (Montgomery et al. 2016; Mariottini 2014).

Cassiopea xamachana Bigelow, 1892

Image credit: Sean Nash, Flickr Common name (s): Upside-down jellyfish Global distribution: Bermuda, Caribbean Sea, Gulf of Mexico, and warm waters of the western Atlantic Ocean. Ecology: It favours muddy substrata of mangroves. Biology Description: It is quite large with a size of about 30 cm in diameter. Umbrella settles on the bottom of the sea floor while its frilly tentacles face upwards. Its saucer-shaped umbrella is relatively flat with a well-defined central depression on the upper surface (exumbrella), the side opposite the tentacles. This depression gives the jellyfish the ability to stick to the bottom of the sea floor while it pulsates gently, via a suction action. There are eight oral arms (tentacles) around the mouth, branched elaborately in four pairs. In this species, there is a central mouth and secondary mouths at the ends of the manubrial branches. Colouration of the animal is greenish grey-blue, due to the presence of the symbiotic zooxanthellae embedded in the mesoglea (jelly) of the body, and especially the arms. While the mobile medusa stage is dioecious (separate males and females), and its polyp stage is sessile and small. 80 4 Biology and Ecology of the Venomous Marine True Jellyfish (Class Scyphozoa)

Food and feeding: The zooxanthellae located in the mesoglea of the jellyfish help it acquire most of its energy through a symbiotic relationship. However, this jellyfish also uses predation. The prey are small organisms, including fish eggs and larvae, copepods, planktonic eggs and a variety of small marine invertebrates. The jellyfish can capture its prey through the use of nematocysts contained within their tentacles. These nematocysts have the ability to sting due to the control of a mechanical and chemical trigger. After injecting a prey with toxins, it is paralysed and feeding becomes easy for the jellyfish. It proceeds to digest its meal, by the manubrial or oral surface, reducing it to fragments that can be ingested through the secondary mouths. Life cycle: In this species, the life cycle consisting of the alternation of two stages, the polyp and the medusa, is found during summer/early fall and all year round, respectively. The polyp is attached to the substrate and is known as a scyphistoma. This reproduces asexually by strobilation, budding off sections from the top, each known as an ephyra (newly strobilated medusa). The adult medusa is lodged on the sea floor most of its time, with the arms facing upwards. In sexual reproduction, fertilization occurs because of the fusion of eggs and sperm. The sperms are released from males and fertilize eggs in nearby females. The eggs develop in the female, and planula larvae are finally released into the water. The planula permanently attaches to the surrounding substrate. After attaching, the planula undergoes metamorphosis into a sessile polyp with tentacles known as a scyphistoma. Asexual reproduction occurs when sufficient food is present. Association: A symbiotic relationship exists between endosymbiotic dinoflagellate Symbiodinium microdraiticum and Cassiopea xamachana. The zooxanthellae reside on the underside of the bell, on the tentacles, so Cassiopea xamachana is held upside-down. Envenomation: The venom of this species showed strong haemolytic activity and produced concentration-dependent haemolysis on sheep and, particularly, human RBCs (Mariottini 2014; Soeiro and Morais https://core.ac.uk/download/pdf/ 62708328.pdf). PLA2/PLA2-like catalytic activity has been detected in several fractions of venom from tentacle nematocysts of this species (Remigante et al. 2018). 4.3 Family Catostylidae 81

4.3 Family Catostylidae

Acromitoides purpurus (Mayer, 1910)

Common name (s): Blue bubbler jellyfish Global distribution: Tropical western central Pacific: Philippines. Ecology: It is a pelagic species. Biology Description: Bell of this species is 115 mm in width and 35 mm in height. Exumbrella is smooth. There are 32 clefts and 16 simple velar lappets. Mouth arms are shorter than the radius of the bell. Lower three-winged portion is five to seven times as long as upper cylindrical portion. Animal is with uniform dark brownish purple colour. Life cycle: Reproductive strategies of this species are unknown. Envenomation: It is a venomous species (Blaxter et al. 1984; Burnett et al. 1996). Its venomology is to be known.

Catostylus mosaicus (Quoy & Gaimard, 1824) 82 4 Biology and Ecology of the Venomous Marine True Jellyfish (Class Scyphozoa)

Image credit: Isobel Bennett, Australian Museum Common name (s): Jelly blubber, blue blubber jellyfish, blue jelly, mosaic sea jelly Global distribution: Tropical Indo-West Pacific: Pakistan, Australia and the Malay Peninsula. Ecology: It occurs in coastal regions often in large swarms. It can also enter intertidal estuaries. Biology Description: Its large bell is creamy white, blue or brown which is due to its pigment produced. Exumbrella is with coarse granulations. There are about 16 lappets in each octant and these are all alike. Arm-disk is somewhat wider than bell radius. There are eight club-like oral arms that each contains several mouths. These mouth arms are about 1.5 times as long as bell radius. This species grows to a diameter of 30–45 cm. Food and feeding: It eats mainly plankton, small fish, some crustaceans and small particles in the ocean water. The mouths of oral arms transport food to the jelly’s stomach. Tentacles also have stinging cells that can capture the food items. Life cycle: As with all true jellies, these blue jellies alternate between a sexual medusa stage and an asexual polyp stage. Adult medusae brood their fertilized eggs and the resulting planula larvae can live for up to 13 months. Within 1–3 months, these larvae can grow to sexual maturity. Food value: People can safely eat this venomous (poisonous) jelly if it has been correctly dried and processed. The Chinese believe that eating jellies will reduce high blood pressure. Dried jellies are popular in many Asian countries, especially Japan, where they are considered a culinary delicacy (Anon. https://animals-and- creatures-that-lived-in-prehistory.fandom.com/wiki/Blue_Blubber_Jelly_ Catostylus_mosaicus). Envenomation: The sting of this venomous species can be painful but generally poses no serious risk to humans (Anon. https://en.wikipedia.org/wiki/Jelly_blubber; Wiltshire et al. 2000). Jouiaei (2016) reported that this species contains toxin proteins containing Stichodactyla toxin (ShK) domain (CRiSPs), cystatins and serine protease inhibitors in its oral arms and tentacles. 4.3 Family Catostylidae 83

Catostylus tagi Haeckel, 1869

Image credit: Flickr Common name (s): Jelly blubber Global distribution: Tropical Indo-Pacific. In Australia, it occurs off the coasts of Queensland, New South Wales and Victoria. It is also native to the Mediterranean Sea and the Atlantic Ocean. Ecology: This pelagic, coastal species can also enter intertidal estuaries. Biology Description: It is a large, hemispherical species with a diameter of 65 cm. Bell is massive, flexible but firm. Surface is smooth, except for shallow forking grooves in peripheral of radius. Marginal lappets are up to eight per octant and there are eight rhopalia. Mouth arms are 8 and are approximately as long as bell diameter. Mouthlets are seen on distal 3/4, tapering neatly to somewhat pointed end and without filaments or clubs. Gonads are rimming the cross-shaped stomach. Colouration of body is variable and can be blue, cream, brown or off-white. Certain specimens can have a reddish or purplish brown exumbrellar grooves. Gonads are red. Food and feeding: It eats both zooplankton and phytoplankton, certain crustaceans and small fish. Biomedical use: Its bell collagen which is made up of 1/3 glycine, water and other amino acids is currently being researched for use as a matrix. 84 4 Biology and Ecology of the Venomous Marine True Jellyfish (Class Scyphozoa)

Envenomation: The sting severity of this jellyﬁsh is mild. It will hurt when it stings but poses no serious threat (Montgomery et al. 2016). Soeiro and Morais (https://core.ac.uk/download/pdf/62708328.pdf) reported on its haemolytic activity. In vitro preliminary haemolytic studies of toxins from the jellyﬁsh Catostylus tagi. Rita Soeiro 1 and Zilda Morais 1, https://core.ac.uk/download/pdf/62708328. pdf

4.4 Family Cepheidae

Cotylorhiza tuberculata (Macri, 1778)

Image credit: Wikipedia Common name (s): Mediterranean jelly, fried egg jellyfish Global distribution: It is commonly found in the Mediterranean Sea, Aegean Sea, Adriatic Sea, Red Sea, Canary Islands, Turkish waters. Ecology: It lives at the sea surface and it is often accompanied by juvenile fish such as horse mackerel (Anon. http://www.cmas.org/news/watch-out-for-the-gelati nous-organisms-of-the-eastern-mediterranean). Biology Description: It is a brown to yellowish medusa with a flattened bell with a raised central portion. Its marginal bell is divided into 16 main lobes which are further subdivided into numerous small lobes. It carries eight oral arms with several projections having violet or purple tips. Food and feeding: It primarily consumes miniscule aquatic organisms, often a mixture of phytoplankton and zooplankton. 4.4 Family Cepheidae 85

Life cycle: In sexual reproduction, females are internally fertilized with sperm from the mouth arm appendages of their male counterparts, and after a gestation period, large numbers of planulae are finally released into the water. Association: The endosymbiotic, photosynthetic algae, zooxanthellae Envenomation: This species may inflict a painful sting and one should be cautious in handling them with bare hands (Turk 1999). From the toxicological point of view, this species was defined as “not very toxic” and “unharmful species causing troubles to bathers when it occurs copiously”. However, large swarmings of this species were reported to cause nuisances in bays and in coastal areas of Greece in summer (Mariottini and Pane 2010). It seems that this jellyfish’s sting is mid, and it has very little or no effect on humans (Montgomery et al. 2016; Williamson et al. 1996).

Marivagia stellata Galil & Gershwin, 2010

Common name (s): Not designated Global distribution: Indian Ocean; Northern Arabian Sea, India and Pakistan; Mediterranean Sea, Tanzania. Ecology: It is a pelagic, planktonic species living in coastal waters and estuaries. Biology Description: It is a translucent bluish-white sea jelly. Bell grows to 12–15 cm in width and it has eight arms. Its exumbrella surface lacks central dome, warts or knobs. It is, however, ornamented with conspicuous pattern of reddish stars, dots and streaks clustered in centre third of exumbrella. Subumbrella lacks ﬁlaments on oral disk and between mouths. It is with approximately nine gelatinous radial ridges per octant, extending from peripheral edge of gastrogonadal region halfway to margin, ending abruptly. Peripheral region of bell is inverted. There are eight oral arms which is shorter than bell radius, triangular in cross section. There are no appendages between mouths. There are eight rhopaliar canals. In life, this medusa is translucent bluish-white jelly, with conspicuous pattern of reddish stars, dots and streaks clustered in centre third of exumbrella. Gonads are pale whitish. 86 4 Biology and Ecology of the Venomous Marine True Jellyfish (Class Scyphozoa)

Food and feeding: Its diet includes small organisms in the water table. The stinging cells on the tentacles are used to capture the prey. Life cycle: Little is known about the reproductive habits of this species. Envenomation: It is a mild stinger and there is not much information about its effects on humans (Montgomery et al. 2016; Anon. https://in.pinterest.com/pin/ 438819557423753355/?lp¼true).

4.5 Family Cyaneidae

Cyanea capillata (Linnaeus, 1758)

Image credit: Dan Hershman, Wikipedia Common name (s): Lion’s mane jellyfish, giant jellyfish, hair jelly Global distribution: Its range of distribution is confined to cold, boreal waters of the Arctic,northernAtlantic and northern PacificOceans. It is common in the English Channel, Irish Sea, North Sea and in western Scandinavian waters south to Kattegat and Øresund. It may also drift into the south-western part of the Baltic Sea. Ecology: It remains mostly very near the surface, at no more than 20 m depth. Their slow pulsations drive them forwards weakly, so they depend on ocean currents to travel great distances. Biology 4.5 Family Cyaneidae 87

Description: It is the largest known species of jellyfish with a diameter of 2.3 m and its tentacles which are about 1200 are 38 m long. Large individuals are often red or purple, while smaller specimens tend to be shades of tannish orange. Bell of this jellyfish is scalloped into eight lobes (lappets), each lobe containing from 70 to 150 tentacles, arranged in four fairly distinct rows. Along the bell margin is a balance organ at each of the eight indentations between the lobes—the rhopalium—which helps the jellyfish orient itself. From the central mouth extend broad frilly oral arms with many stinging cells. Food and feeding: The lion’s mane jellyfish uses its stinging tentacles to capture, pull in and eat prey such as zooplankton, small fish, ctenophores and moon jellies. Predators: Predators of the lion’s mane jellyfish include seabirds, larger fish such as ocean sunfish, other jellyfish species and sea turtles. The leatherback sea turtle feeds almost exclusively on these three jellyfishes in large quantities during the summer season around Eastern Canada. Association: In the open ocean, lion’s mane jellyfish act as floating oases for certain species, such as shrimp, medusafish, butterfish, harvestfish and juvenile prowfish. They provide both a reliable source of food and protection from predators. Life cycle: Like other jellyfish, lion’s manes are capable of both sexual reproduc tion in the medusa stage and asexual reproduction in the polyp stage. They have four different stages in their year-long lifespan, viz. a larval stage, a polyp stage, an ephyrae stage and the medusa stage. The female jellyfish carries its fertilized eggs in its tentacle, where the eggs grow into larvae. When the larvae are old enough, the female deposits them on a hard surface, where the larvae soon grow into polyps. The polyps begin to reproduce asexually, creating stacks of small creatures called ephyrae. The individual ephyra breaks off the stacks, where it finally grows into the medusa stage and becomes a fully grown jellyfish. Envenomation: These jellyfishes cause temporary pain and localized redness. In normal circumstances, and in healthy individuals, their stings are mils and are not known to be fatal. However, at deep water, severe stings can also cause panic followed by drowning (Montgomery et al. 2016; Anon. https://en.wikipedia.org/ wiki/Lion%27s_mane_jellyfish). The crude venom containing the toxins-CcTX-1 and CcNT from mesenteric tentacles of large animals showed haemolytic activity by inducing more pronounced RBC lysis (Mariottini 2014; Frazão and Antunes 2016). Contact with the tentacles of this species may produce a burning feeling which may become more severe (Dong et al. 2010). Remigante et al. (2018) reported that the tissue homogenates of this species showed high PLA2 (Phospholipase A2) catalytic activity. The venom from Cyanea capillata has cytotoxic, cardiotoxic, haemolytic, neurotoxic and phospholipase A activities. Two kinds of toxins from the venom have been isolated. The first isolated toxin, CcTX1, was found to be cytotoxic to human hepatocyte cells and the second, CcNT, a neurotoxin, was purified based on toxicity to mouse neuroblastoma and was found to be neurotoxic. Unfractionated venom was toxic to cells from rainbow trout, mouse neuroblastoma, human hepatocytes and rat renal tubular epithelial cells shown in in vitro and in vivo tests (Nordesjö 2016). 88 4 Biology and Ecology of the Venomous Marine True Jellyfish (Class Scyphozoa)

Cyanea ferruginea Eschscholtz, 1929

Common name (s): Not designated Global distribution: Paciﬁc island of North Asia; China. Description: It largely resembles Cyanea capillata. No other information is available. Envenomation: As lion’s mane jellyﬁsh (Cyanea capillata), the stings of this species also cause severe pain and can lead to dangerous systemic effects, including Irukandji-like syndrome (Blaxter et al. 1984).

Cyanea lamarckii Peron & Lesueur, 1810

Common name (s): Blue jellyfish, bluefire jellyfish Global distribution: Western Pacific around Japan. Ecology: It is a pelagic, planktonic species. Biology 4.5 Family Cyaneidae 89

Description: Bell of this species can grow up to 30 cm in diameter. Hollow marginal tentacles arise from the underneath of the bell. These are arranged in eight horseshoe- or rectangular-shaped groups each with 40–60 tentacles. Beneath the bell is a short thick manubrium merging onto four wide membranous and folded curtain- like oral lips which may be yellowish and fade to white at their extremities. It has thick and frilly oral arms that are slightly shorter than the diameter of the bell. Sense organs in the bell are protected by a long exumbrellar extension which forms a hood. Its colour varies from translucent through pale yellow, pale brown, pale grey to light blue or purple. It has four interradial folded gonads that hang freely downwards beneath the bell surface. Food and feeding: This species takes a diet of phytoplankton or zooplankton as well as the eggs and larvae of other aquatic animals such as fish. Envenomation: Purified cnidocyst extracts of this species showed haemolytic activity (Mariottini 2014). Sting severity of this species is mild (Montgomery et al. 2016). The venom from cnidocyst extracts prepared from mesenteric and fishing tentacle of this species showed PLA2/PLA2-like catalytic activity (Remigante et al. 2018). Frazão and Antunes (2016) reported on the occurrence of a toxin CIGP from this species.

Cyanea nozakii Kishinouye, 1891 Image not available Common name (s): Ghost jellyfish. Global distribution: Northern Pacific Ocean: coasts of China and Japan. Ecology: It is coastal, pelagic species. It is showing a greater tendency to appear in large numbers as swarms. Biology Description: Medusoid stage of this species has a distinctive flat-topped bell which can grow to a diameter of 50 cm. Bell is usually cream or pale yellow in colour with a dark centre and a translucent rim. It has eight large marginal lobes and eight bundles of thread-like marginal tentacles. There may be a hundred or more tentacles in each bundle which are either translucent or a reddish colour and can extend for 10 m. Under the centre of the bell is the manubrium. Mouth is surrounded by a tangled mass of rusty brown or orange oral tentacles. Association: A number of species of juvenile fish such as razorbelly scad (Alepes kleinii) and Malabar trevally (Carangoides malabaricus) associate with this jellyfish, making use of the protection provided by its stinging tentacles. Further, the stalked barnacle Alepas pacifica hangs from the margin of the bell of this species. Envenomation: It is one of the most dangerous stingers in the coast of China. Hundreds of thousands of people would be stung every year and victims suffered a severe pain, itch, swelling, inflammation, wheal and even more serious consequence (Li et al. 2016). A concentration-dependent haemolytic activity on chicken RBCs at pH optimum of 7.8 was also observed in the nematocyst venom of this species (Mariottini 2014). 90 4 Biology and Ecology of the Venomous Marine True Jellyfish (Class Scyphozoa)

PLA2/PLA2-like catalytic activity and metalloproteinase enzymatic activity have been detected in the crude venom from nematocysts of this species (Remigante et al. 2018).

Cyanea purpurea Kishinouye, 1910 Image not available Common name (s): Lion’s mane jellyfish Global distribution: Subtropical Indo-West Pacific: India and Japan. Ecology: It is a planktonic species Biology Description: Bell of this species attains a maximum diameter of 30.0 cm. Animal is coloured lilac, with honey-brown spots over the upper surface. A dense cluster of filmly mouth parts and hundreds of long tentacles are seen. Envenomation: Stings of this species cause instantaneous pain with rapid development of erythema and weals. One sting on the forearm produced rows of erythematous papules 2 mm across spaced 6 mm apart. Though the pain may subside over 30–60 min, it may persist for a few hours if sensitive areas such as lips are stung. While erythema subsides over about 3 h, the weals take a few days to resolve completely, during which time they are mildly pruritic (Anon. file:///C:/Users/ Ramesh/Downloads/6443-22869-1-PB.pdf). This venomous species has been reported to occasionally harm bathers and divers, but its sting usually causes only transient pain (Blaxter et al. 1984; Bambaradeniya and Karunaratne 2006).

4.6 Family Drymonematidae

Drymonema dalmatinum Haeckel, 1880

Common name (s): Stinging cauliﬂower, big pink jellyﬁsh Global distribution: Gulf of Mexico, Mediterranean Sea, Caribbean Sea and off the Atlantic coast of South America. 4.7 Family Linuchidae 91

Ecology: This is a coastal pelagic species. Biology Description: It has a ﬂat umbrella which can reach up to 1 m. Its oral arms are thin and when extended they can reach a length greater than the bell’s diameter. Gastro- vascular pouches are as numerous as marginal lappets and are narrow, elongate and forking in basal region. Ground colour of bell is probably somewhat pale. However, reddish-white, milk-white, light rose to violet, and yellowish brown to pale golden- yellow-coloured specimens are also available. Tentacles are translucent and colourless but are also noted as white with inner canal reddish or pale golden yellow. Food and feeding: These animals feed on other jelly species such as Aurelia spp. by reeling them in with their long tentacles. It is considered as the most efﬁcient jellyvorous jelly, as it can digest its prey within 2–3 h. In periods of increased populations of its prey, it forms huge swarms. Envenomation: Its sting severity is high and this species is considered venomous with severe effects to humans (Montgomery et al. 2016; Anon. http://www.oceanog raphy.ucy.ac.cy/medusa/species/descriptions/drymonema.html).

4.7 Family Linuchidae

Linuche unguiculata (Schwartz, 1788)

Common name (s): Thimble jellyfish, sea thimble, button jellyfish Global distribution: Subtropics and tropics; western Atlantic Ocean; West Indian and Bahama regions. Ecology: It lives in the epipelagic (surface to 200 m), mesopelagic (200–1000 m), bathypelagic (1000–4000 m) or abyssopelagic (4000–6000 m) regions. It forms 92 4 Biology and Ecology of the Venomous Marine True Jellyfish (Class Scyphozoa) swarms in warm seas near the surface of the water. Aggregations of this species have been reported covering a million square metres. Biology Description: Its umbrella medusa has a radially symmetric body shape. Eight gonads (arranged in pairs) in four gastric pouches connect to 16 peripheral stomach pouches, which extend into 16 blunt, oval, marginal lappets. Between the folds of the lappets are an alternating eight tentacles and eight rhopaliums (sense organs). Tentacles are quite short and are not easily noticeable. No marginal ring canal exists. There is one mouth in the centre on the underside of the medusa umbrella. Its thimble-shaped umbrella has a width of 16 mm and a height ranging from 13 to 20 mm. Polyp from this species can be colonial or solitary. Polyp is composed of hard, thin tubes of chitin, taking on a hydra-like stalk form. Branched polyp can grow to a height of 150 mm. Food and feeding: This jellyfish feeds on plankton, drawing a water current past its outstretched tentacles by pulsating the bell. When edible zooplankton are encountered, they are immobilized by the cnidocytes (stinging cells) and are passed by the tentacles to the mouth on the underside of the bell. Predators: Thimble jellyfish are consumed by fish, sea turtles and other predators. Life cycle: Linuche unguiculata is dioecious, but not sexually dimorphic. During reproduction, the male releases sperm out of its mouth into the open seawater. By way of cilia currents, some of the swimming sperm are swept into the female’s mouth and then into the female’s gastric pouch. Fertilization is internal. Early embryonic development of the zygote starts in the open seawater or in brood pouches along the oral arms of the female parent medusa. Finally, a ciliated planula larva develops, settles and forms a hydra-like scyphistoma. The scyphistoma may reproduce asexually to form a colonial polyp or it may form a strobila stack of ephyrae buds. Ephyrae break from the strobila to form mature medusa jellyfish. Association: Symbiotic zooxanthellae attach to the surface of L. unguiculata, giving it an overall brownish colour. Underneath the zooxanthellae, the umbrella has a transparent outer coating. The umbrella’s inside surface is white with spots of green and brown. Envenomation: Larvae of the thimble jellyfish are the most common cause of seabather's eruption in the Caribbean and the Gulf of Mexico. This is an itchy rash of small red papules that develops in the areas that were covered by the bather’s swimwear or hair (Schmitt and de Haro 2013; Anon. https://en.wikipedia.org/wiki/ Thimble_jellyfish). Tibballs et al. (2011) reported that contact with this species is not painful, but a prickling or stinging sensation may be experienced while the victim is in the water followed later by severe itching. This toxic component of the illness is followed by an immunological component consisting of an urticarial eruption and a distressing dermatitis which may last many days to several weeks. 4.8 Family Lobonematidae 93

4.8 Family Lobonematidae

Lobonema smithii ( ¼ Lobonema mayeri)

Common name (s): Malaysian white type edible jellyfish Global distribution: Tropical Indo-West Pacific: Indian Ocean; Philippines. Ecology: It is a planktonic species. Biology Description: Bell of this species is flatter than a hemisphere. It is 23.6 cm wide, thick, tough and rigid. Exumbrella is with erect, gelatinous papillae; they are largest and most abundant at centre and are 3.5 to 4 cm long, pointed, with nematocysts. There are four velar lappets in each octant and are 9 to 10 cm long, tapering and pointed. Its eight mouth arms are 15 cm long and are with numerous long spindle- shaped and thread-like appendages which are 70–100 mm long. There are 16 radial canals. General colour of the medusa in formalin is milky grey, and the mouths and gonads are darker than other parts. Commercial use: Type A gelatin produced from the desalted dried jellyfish of this species can be used as an alternative source of gelatin for food applications (Rodsuwan et al. 2016). Edible and therapeutic values: This jellyfish is edible. Further, this species serves as an antioxidant agent and collagen stimulator in wound healing process (Assaw et al. 2016). Envenomation: This venomous species has been reported to inflict a very unpleasant sting, but it was not dangerous. It produced no immediate stinging sensation and the symptoms were of less intensity and duration (Burnett et al. 1996; Blaxter et al. 1984). 94 4 Biology and Ecology of the Venomous Marine True Jellyfish (Class Scyphozoa)

4.9 Family Lychnorhizidae

Lychnorhiza lucerna Haeckel,1880

Common name (s): Marbled jellyfish Global distribution: Tropical south-west Atlantic: Argentina, Brazil and Fr Guiana. Ecology: It occurs in shallow coastal habitats and estuaries; it often becomes stranded on beaches. Biology Description: When small, this species has a hemispherical bell, but this becomes flattened into a saucer shape as the jellyfish grows. In very large specimens, the bell attains a maximum diameter of 45 cm and is dish-shaped. Upper surface is flexible and thin and is covered in low conical projections. There are many small, triangular lappets round the periphery. Hanging under the bell there are four pairs of oral tentacles. There is no central mouth. Stomach occupies most of the interior of the bell, and there are a ring of small cream or white gonads round its edge. Colouration of this jellyfish varies, but in general, the bell is translucent and colourless or a pale shade of buff, sometimes with irregular streaks of light brown. Lappets round the edge of the bell are darker brown and the lower parts of the oral tentacles may be brown. Life cycle: It has a complex life cycle with an alternation of sexual and asexual stages. Medusoid stage is gonochoristic (i.e. either male or female). The fertilized eggs hatch into planula larvae which settle and undergo metamorphosis into sessile polyps, known as a scyphistomae, with four tentacles. These grow larger, and after a series of moults have 22 tentacles. They develop cysts from which new polyps known as ephyrae grow. These develop transverse constrictions and separate from 4.10 Family Mastigiidae 95 the original polyp by strobilation. Ephyrae develop into juvenile medusae after a period of about 15 days. Association: Lychnorhiza lucerna has associations with the parasitic flatworm Dibothriorhynchus dinoi, shrimps Periclimenes spp., the Atlantic bumper fish, Chloroscombrus chrysurus and the bluntnose jack, Hemicaranx amblyrhynchus. Young spider crabs, Libinia ferreirae and Libinia spinosa, use the inner side of the bell as a nursery where they are safe from predation. Others: This species is a nuisance to shrimp trawls as short 10-min trawls could catch dozens of kilograms of this species. This species has therefore been reported to cause fishery losses and economic losses to trawlers (Nagata et al. 2009). Envenomation: It is reported that the nematocysts of this species has little ability to pierce the human skin (Resgalla et al. 2005; Burnett et al. 1996). This venomous jellyfish has been reported to cause cutaneous eruptions following contact. Further delayed reactions are said to be severe (Remigante et al. 2018).

4.10 Family Mastigiidae

Phyllorhiza punctata von Lendenfeld, 1884

Common name (s): Floating bell, Australian spotted jellyfish, brown jellyfish, white- spotted jellyfish 96 4 Biology and Ecology of the Venomous Marine True Jellyfish (Class Scyphozoa)

Global distribution: Warm temperate seas; Tropical Indo-Pacific, western Atlan- tic and the Mediterranean. Ecology: This neritic species is often abundantly aggregated in coastal nearshore and lagoon waters. This euryhaline species is often be found swimming near the surface in murky waters near estuaries in harbours and embayments; also found in mangroves. Biology Description: Umbrella or bell of this species is bluish brown and is nearly semi- spherical; about half as high as broad and punctuated by white crystalline inclusions, giving the appearance of spots. There are eight radial canals which communicate directly with the stomach and there are eight thick transparent branching rhopalia (oral arms) which terminate with large brown bundles of stinging cells. Fourteen lappets are found in each octant of the umbrella. It is 45–60 cm in bell diameter. Subgenital ostia are wider than their height, and the circular subumbrella muscles are interrupted by the eight radial canals. Food and feeding: Its main food source is zooplankton. Life cycle: Reproduction in P. punctata is unique. In the initial stage of life—the polyp stage—the polyp is asexual. It reproduces by multiplying itself various times, creating a larger hatch than the original that the mother had created. The next stage— the medusa stage—is when the jellyfish becomes sexually reproductive. The male shoots his sperm into the water and the female collects the sperm in her mouthlets and filter them to her reproductive organs. There they grow into polyps where they are eventually dropped to the bottom of the ocean where they grow and begin to reproduce on their own. This jellyfish has caused much destruction to fisheries and ecosystems. Association: The phenomenon commensalism (a long-term biological interaction (symbiosis) in which members of one species gain benefits while those of the other species neither benefit nor harmed) exists between this species and Charybdis feriata megalopae. Envenomation: While this species is not overly dangerous to humans, it holds a mild venom that can cause discomfort (Montgomery et al. 2016; Anon. www.news. com.au/travel/travel-updates/australian-spotted-jellyfish-phyllorhiza-punctata- invade-spanish-beaches/news-story/7600460e5a85e34016832cd1291995e1? sv¼15ad0682e9f0b947de3ae5f631b59df2). Anon. (http://www.cmas.org/news/watch-out-for-the-gelatinous-organisms-of- the-eastern-mediterranean) reported that this species may cause slight burning sensation and complaints like itching and tingling. It has only a mild venom and is not considered a threat to humans. The extract of the tentacles of this species has shown PLA2/PLA2-like catalytic activity (Remigante et al. 2018). Frazão and Antunes (2016) reported on the presence of saxitoxin, gonyautoxin-4, tetrodotoxin, and brevetoxin-2 in this species. 4.12 Family Paraphyllinidae 97

4.11 Family Nausithoidae

Nausithoe punctata Kolliker, 1853

Common name (s): Coronate scyphozoan jellyfish Global distribution: Tropical circumglobal; Adriatic Sea. Ecology: It is an offshore species; depth range is 0–1000 m. Biology Description: Bell of this species is tiny, discoid and thick, with fine nematocyst— warted surface and crenate coronal groove. Disc is flat with a maximum diameter of 15 mm; its central region is wider than its height. Coronal groove is prominent, crenate and is delimiting central half of disc. There are 16 marginal lappets with alternating 8 thick tentacles and 8 prominent rhopalia in clefts between. Radial grooves are running to lappets and are separating thick pedalia. Tentacle clefts and rhopalial clefts are about equal in depth. Circular muscle is narrow and is less than 1/3 lappet length in radial extent. There are 8 gonads, spaced apart and are oval to rigidly elongate in outline. Jelly is translucent, and it is milky, greenish or light brownish. Gonads (male) are bright yellow and that of female are brown to red. Pigment patches between gonads and small crystalline spots on exumbrella are seen. Food and feeding: It feeds on zooplankton. Envenomation: It is a venomous jellyfish and its sting severity is mild (Montgomery et al. 2016).

4.12 Family Paraphyllinidae

Paraphyllina ransoni Russell, 1956 Image not available Common name (s): Not designated Global distribution: Subtropical Paciﬁc, Atlantic and the Mediterranean: Liberia, USA and Canada. 98 4 Biology and Ecology of the Venomous Marine True Jellyfish (Class Scyphozoa)

Ecology: It is a deep-water species. Biology Description: Bell of this species is transparent and dome-shaped with prominent coronal groove. Exumbrella is with nematocyst warts, and mesoglea is fairly thick. There are 16 pedalia, 16 marginal rounded lappets and 4 perradial rhopalia. Among its 12 solid, marginal tentacles, 8 are adradial and 4 are interradial in position. Subumbrellar coronal muscle is continuous and is prominent. Stomach is attached to subumbrella by four interradial gastric septa, forming four pockets that separate subumbrella from manubrium. Manubrium is with four mesogleal perradial reinforcements and crenate margin. There are eight gonads which are W-shaped. Bell reaches a diameter of 7.5 cm. Colour of stomach is deep chocolate-red and rest of the body is colourless. Envenomation: Sting severity of this venomous species is mild (Montgomery et al. 2016).

4.13 Family Pelagiidae

Chrysaora achlyos Martin, Gershwin, Burnett, Cargo & Bloom, 1997

Image credit: Monterey Bay Aquarium, Wikimedia Commons. Common name (s): Black sea nettle, black jellyﬁsh, sarlacc jellyﬁsh. 4.13 Family Pelagiidae 99

Global distribution: Pacific Ocean: from Monterey Bay in the north, down to southern Baja California and Mexico; British Columbia. Ecology: It is occasionally seen in large numbers in surface waters. Biology Description: It is quite massive, with a bell diameter up to 1 m and its oral arms are extending to 6 m. Bell colour is a distinctive opaque dark purple to nearly black, with the margin having a lighter brown reticulated pattern. Four gonads are attached to finger-like projections that extend through subumbrellar openings (the ostia). There are eight marginal sense organs which are spaced around the bell margin after every set of three tentacles. Food and feeding: It is carnivorous, feeding on zooplankton and other jellyfish. Nettles immobilize and obtain their prey using their stinging tentacles. Life cycle: Like other jellyfish, this species alternates body forms between generations, between a polyp and a medusa. The polyp asexually produces a jellyfish, which then sexually produce more polyps. Envenomation: On humans, this species will most likely cause a non-lethal, but painful stinging sensation which can last for 40 min (Anon. https://en.wikipedia.org/ wiki/Chrysaora_achlyos). Anon. (https://bio113.weebly.com/chrysaora-achlyos.html) reported that the venom from the nematocysts of this species is fatal to mice. However, in humans, its stings are relatively mild and associated symptoms disappear in less than an hour. Mariottini (2014) reported that this species showed haemolytic activity (breaking down of red blood cells—erythrocytes, causing anaemia if there is no compensation from the bone marrow). Radwan et al. (2000) reported that the nematocyst venoms from both oral arms and lappets of this species produced mouse lethality, haemolysis and hepatocyte toxicity.

Chrysaora colorata (Russell, 1964) ( ¼ Pelagia colorata)

Image credit: Wikimedia Commons Common name (s): Purple-striped jellyﬁsh, purple-striped sea nettle Global distribution: Off the coast of California in Monterey Bay. 100 4 Biology and Ecology of the Venomous Marine True Jellyfish (Class Scyphozoa)

Ecology: It is an oceanic and continental slope water species. Biology Description: Bell (body) of this jellyfish is up to 70 cm in diameter and is with a radial pattern of stripes. Tentacles vary with the age of the individual, consisting typically of eight marginal long dark arms and four central frilly oral arms. When it is extremely young, it has a pinkish colour and its tentacles are long and dark maroon. At the adult stage the dark maroon colour of the tentacles starts to fade and the purple appears as stripes on the bell. Food and feeding: It feeds on small crustaceans, ctenophores, fish eggs and larvae and other gelatinous zooplankton. When the prey touches a marginal tentacle of this species, stingers are immediately discharged to paralyse prey and marginal tentacle bends inward to the nearest oral arm. The oral arm is used to transport prey to the gastrovascular cavity and to catch motionless prey. Predators: Sunfish, sea turtles, leatherback turtles. Association: Young Cancer crabs often make home in the jellyfish and eat the parasitic amphipods that feed on and damage the jellyfish. Envenomation: The strong sting of this venomous jellyfish is extremely painful to humans (Blaxter et al. 1984; Anon. https://en.wikipedia.org/wiki/Chrysaora_ colorata, https://scripps.ucsd.edu/zooplanktonguide/species/chrysaora-colorata). Anon. (https://purplestripedjellyfish.weebly.com/dangerous.html) reported that the purple-striped jelly stingers do hurt, but they are rarely ever fatal. When this jellyfish is threatened by another encounter, it applies pressure inside the nematocyst, makes the threads unfold and spring out to the foreign object. They shoot out like tiny little darts, leaching on to the skin or flesh, then they extract the venom. The sting of this jellyfish cannot kill humans, but it will though cause pain, skin rashes, fever and muscle cramps.

Chrysaora fuscescens Brandt, 1835 4.13 Family Pelagiidae 101

Image credit: James Draginda, PandasThumb Common name (s): Pacific sea nettle, West Coast sea nettle Global distribution: Pacific and Indian oceans: Japan and Siberia; from northern Alaska to Mexico. Ecology: This epipelagic species may form large groups just offshore on the open coast, and many may strand themselves on the beach. Biology Description: This scyphomedusa has an amber-coloured bell which is darkest near the margin. It may have an indistinct, pale star pattern radiating to the margin as well. It has 24 tentacles which are long and brown and start individually between the lappets. There are three tentacles between each rhopalium (it has 8 rhopalia). Oral arms are long and strongly spiralled when contracted though they may be straight when relaxed. Oral arms have crenulated edges. Bell of this species is up to 30 cm in diameter and its tentacles/oral arms may reach to 2.4 m. Food and feeding: This carnivorous species feeds on a variety of zooplankton, including other jellyfish, as well as fish eggs, baby and adult fish, crustaceans and other floating animals. By spreading out its tentacles like a large net, this sea nettle is able to catch food as it passes by. When prey brushes up against the tentacles, thousands of nematocysts are released, launching barbed stingers which release a paralysing toxin into the quarry. The oral arms begin digestion as they transport the prey into the sea nettle’s mouth. Predators: It is the prey to many marine birds and large fish. Life cycle: This species has a very complex life cycle made up of five stages. Its lifecycle begins when males broadcast sperm into the water and the females catch the sperm to fertilize the eggs she has produced and is holding in her mouth. Fertilized eggs remain attached to the mother’s oral arms and grow into planulae larvae. The planulae then grow into flower-shaped polyps, which are released into the ocean. Each polyp attaches to a solid surface and undergoes asexual reproduction through which it makes new polyps by budding. After the new polyps are fully formed, they are released into the ocean and start to change shape, looking more like the adult nettle. These juveniles develop a bell, arms and tentacles and become adults. Envenomation: This species can sting a human who comes into contact with its tentacles. Though the toxin it releases is generally harmless to most people, the sting can be painful (Anon. http://www.robinsonlibrary.com/science/zoology/cnidaria/c- fuscescens.htm). Ponce et al. (2016) reported that this species possesses a painful sting that can cause harmful reactions in humans including burning sensation, blisters, skin redness, headaches, cramps and lachrymation. 102 4 Biology and Ecology of the Venomous Marine True Jellyfish (Class Scyphozoa)

Chrysaora helvola Brandt, 1838

Image credit: Wikimedia Commons Common name (s): Indonesian sea nettle Global distribution: South Pacific Ocean. Ecology: It is a planktonic species. Biology Description: Bell of this species is 100–300 mm wide and is hemispherical or flatter. Exumbrella is smooth. There are 32 marginal lappets which are oval in shape. Tentacles numbering 24 are flat, ribbon-like. Its four mouth arms are 4 m long and are with broad frilly margin. Of the 16 gastric pouches, rhopalar ones are oval and tentacular ones are rectangular. Bell is yellowish brown or reddish yellow with 32 rayed chestnut brown stars. Marginal lappets and mouth arms are speckled with rusty red. Tentacles are dark rusty red. Life cycle: Its reproductive strategies are unknown. 4.13 Family Pelagiidae 103

Envenomation: The nematocysts venom of this severe stinger has been reported to possess apoptosis activity accompanied by uncoupling of oxidative phosphorylation (Qu et al. 2016; Blaxter et al. 1984).

Chrysaora hysoscella (Linnaeus, 1766)

Image courtesy: Wikimedia Commons Common name (s): Compass jellyfish, sea nettle Global distribution: Cold and temperate regions of the Northeast Atlantic: Celtic, Irish and North Seas; southern Atlantic Ocean: Mediterranean Sea, South Africa and False Bay. Ecology: It inhabits shallow coastal waters from surface waters to just above the seabed; it is rarely found deeper than 30 m from the surface. Biology Description: It is a true jellyfish displaying radial symmetry. As an adult, the compass jellyfish has a maximum diameter of 38 cm. It usually has 16 brown elongated V-shaped markings on the translucent yellow-white bell. Markings surround a central brown spot and resemble the face of a compass, hence the common name compass jellyfish. It is usually coloured yellowish white, with some brown. Its 104 4 Biology and Ecology of the Venomous Marine True Jellyfish (Class Scyphozoa)

24 tentacles are arranged in eight groups of three. Each tentacle has stinging cells. Mouth is located between the oral arms at the centre of the underside of the bell. A sense organ is located between each group of tentacles, which can perceive changes in light and helps the jellyfish determine and maintain its position in the water column. It has four oral arms which are longer with a folded, frilly appearance. Food and feeding: Compass jellyfish are carnivores, consuming other marine invertebrates and plankton.[They feed on a variety of benthic and pelagic organisms including dinoflagellates, copepods, crustacean eggs, larval fish and chaetognaths]. They stun and capture their prey with stinging cells on their tentacles. The oral arms facilitate movement of captured prey into the oral opening. Predators: Compass jellyfish are known to be consumed by the leatherback sea turtle and ocean sunfish. Life cycle: It has both sexual and asexual reproduction throughout its development. Mature individuals reproduce sexually by broadcast spawning. Males release sperm from their mouths into the water column. Females fertilize the sperm and can fertilize sperm from multiple male partners. The larvae released from the female settle as benthic polyps that reproduce asexually. The polyps release multiple ephyrae (the earliest forms of the medusoid stage) through strobilation. Association: Adults of this species are highly susceptible to the parasite Hyperia medusarum. Envenomation: Stings of this species are painful and sometimes deadly to humans. One should therefore be cautious in handling this species with bare hands (Turk 1999; Anon. https://en.wikipedia.org/wiki/Chrysaora_hysoscella). Its sting has been reported to cause pruritus, erythema, oedema and burning. These complaints spontaneously disappear in a few hours. In some cases, pruritus, erythema and oedema may occur after 48 h of the contact (Anon. http://www.cmas. org/news/watch-out-for-the-gelatinous-organisms-of-the-eastern-mediterranean). Montgomery et al. (2016) reported that the sting severity of this venomous species is high with cutaneous symptoms such as wheals and punctuate, and erythematous rash. 4.13 Family Pelagiidae 105

Chrysaora lactea Eschscholtz, 1829

Common name (s): Sea nettle Global distribution: Tropical western Atlantic: Cuba to Argentina, Brazil and Caribbean Sea. Ecology: It is a planktonic species. Biology Description: Bell of this species is 60–800 mm wide and is almost hemispherical. Mesoglea is thin and flexible. Exumbrella is finely granulated with very small nematocyst warts. There are 48 marginal lappets which are rounded. Its 24–40 tentacles are as long as bell diameter. There are four mouth arms which are broad, delicate, with frilly margin and is slightly coiled at distal end. Its 16 gastric pouches are uniformly wide centrally, and the tentacular pouches are enlarged distally. Its four gonads are semicircular and much folded. Live specimens are milky white with small brown spots on exumbrella and mouth arms. Nematocysts on exumbrella are milky yellow. Some specimens of this species have also been observed with a radial pattern of brownish triangles. Rhopalia are yellowish and gonads are dull milky pink. Life cycle: It has a planula larva which is elongated, pear shaped, 0.14–0.2 mm long and whitish. This larva is transformed into scyphistoma which is conical to goblet- shaped, 2.2 mm high and its oral disc is 1.2 mm wide. There are 12–21, typically 16, tentacles which are five times as long as the polyp height and are whitish to cream. The resulting podocysts are trapezoid, 0.2–0.3 mm wide and yellowish brown. The strobila is with 2–10 ephyrae which are whitish. Strobilation is lasting about 10 days, resulting in the liberation of ephyrae. Each ephyra after its release is with 8 arms/lobes, 16 marginal lappets and 8 rhopalia. It is 1 mm wide and is transparent. Envenomation: Over 20,000 envenomations of this species have been reported in the State of Paraná (southern Brazil) during the austral summer of 2011–2012. 106 4 Biology and Ecology of the Venomous Marine True Jellyfish (Class Scyphozoa)

Envenomations of this species were considered mild. But almost 600 cases were treated in emergency services, with either toxic or allergic reactions, some with systemic manifestations (Marques et al. 2014; Anon. http://dryades.units.it/jelly/ index.php?procedure¼taxon_page&id¼&num¼77).

Chrysaora melanaster Brandt, 1838

Image credit: Wikipedia Common name (s): Seanettle Global distribution: Pacific Ocean: from Japan north to the Bering Sea. Ecology: This neritic species resides in epiplegic (surface waters) to about 100 m depth and over basins. Biology Description: This jelly’s bell can be white to dark purple/red, with dark lines radiating from the top of the bell. There are 24–32 long orange-red tentacles which may stretch more than 3 m. Its four long lips are curtain-like. Marginal rhophilia (sense organ) are 8 in number and are spaced between 32 lappets. There are 16 dark brown/black radiating streaks on subumbrella between 8 stomach pouches. Food and feeding: Diet of this species includes copepods, larvaceans, other jellies, larger zooplankton and small fish. Predators: Sea turtles and other jelly-eating animals such as tuna, sunfish, butterfish and spiny dogfish keep this jelly population in balance. Life cycle: An obligate benthic phase that strobulates (buds) to release ephyrae larvae which mature into adult. These adults release eggs and sperm, and fertilized eggs settle to seafloor to produce a small non-colonial benthic form. 4.13 Family Pelagiidae 107

Envenomation: The tentacles of this venomous species can produce a nasty sting to humans (Blaxter et al. 1984; http://www.arcodiv.org/watercolumn/cnidarian/ Chrysaora_melanaster.html). Anon. (https://www.aqua.org/Experience/Animal-Index/northern-sea-nettle) reported that although this species is not very venomous, its sting can cause an allergic reaction in some people. Its nematocysts (i.e. stinging cells) are powerful and are capable of causing serious skin irritation and burning sensations.

Chrysaora quinquecirrha (Desor, 1848)

Image credit: Wikimedia Commons Common name (s): Atlantic sea nettle, East Coast sea nettle Global distribution: Tropical and subtropical parts of the Atlantic, Indian and Paciﬁc Oceans. It is frequently seen along the eastern Coast of the United States, such as the Chesapeake Bay. Ecology: These sea nettles are found in high-salinity open ocean, lower salinity of bays and brackish water of estuaries. Biology 108 4 Biology and Ecology of the Venomous Marine True Jellyfish (Class Scyphozoa)

Description: Bell of this species is somewhat saucer-shaped. Four thick, long, lacy oral arms hang from the bell margin, which is scalloped into shallow lobe-like structures called lappets. There are 4–40 long thread-like tentacles on the bell margin which alternate with marginal sense lobes (rhopalia) between lobes. While pink nettles usually have 10 tentacles and white ones have 21. Manubrium extends well below the bell margin. Its four gonads are heart-shaped. Radial canals are present. Bell colouration varies by location. Open ocean forms are pink to reddish maroon with radiating red stripes that may extend down the yellow tentacles. Specimens in the low salinity waters of estuaries have a white bell and no radial stripes. Gonads can be pink, light grey, yellow or clear. Bell diameter may vary from 10 cm to 25 cm and height from 5 cm to 19 cm. Food and feeding: Like other sea nettles, this species is a voracious carnivore. Its preferred prey is ctenophores (comb jellies) (Mnemiopsis spp.) It also eats small fishes, copepods, young minnows, mosquito larvae, bay anchovy eggs and other zooplankton. Predators: It is preyed by mainly sea turtles, ocean sunfish and larger jellyfish. Life cycle: This sea nettle becomes sexually mature when the bell diameter is 3.8 cm in diameter. An adult female produces eggs that are held in its oral arms around its mouth. The male jelly releases sperm into the water, and the female uses her oral arms and tentacles to bring in sperm to fertilize her eggs. The fertilized eggs remain on the oral arms until they develop into ciliated larvae, the planulae which drop off the oral arms and are swimming freely for settlement in the underside of oyster shells. They are now known as sessile planocysts which undergo asexual or sexual mode of reproduction. They either bud off non-motile clones of themselves or a phase called strobilation occurs. Miniature medusa-like structures called strobilia are formed on a stalk. The strobilia bud off as individual eyphyra that develop marginal lobes, rhopila, tentacles, elaborate oral arms, and finally, the bell shape of the adult medusa, the form in which sexual reproduction occurs. Each polyp produces up to 45 ephyrae. Envenomation: The sea nettle’s sting is rated from “moderate” to “severe”, and it is not potent enough to cause human death, except by allergic reaction. While the sting is not particularly harmful, it can cause moderate discomfort to any individual stung. On humans, this will most likely cause a non-lethal, but nevertheless painful rash typically persisting for about 20 min. Some earlier cases from the Philippines reportedly had more severe effects and one account described a sting causing vascular insufficiency, and another mononeuritis (Wikipedia). Shryock and Bianchi (1983) reported that the venom of this species formed a monovalent cation channel in cardiac skeletal muscle surface membranes that allowed a rapid influx of sodium into the cell. Mariottini (2014) reported that the nematocyst venom of this species containing different haemolysins showed more haemolytic potency on human RBCs. Remigante et al. (2018) reported on the presence of deoxyribonucleases in the venom of this species. These enzymes participate in a variety of metabolic functions including genetic recombination. 4.13 Family Pelagiidae 109

Houck et al. (1996) and Ponce et al. (2015) reported that the venom of this species is toxic to the cardiac, respiratory, renal and hepatic systems in animal models. According to Ponce et al. (2016), the venom of this species showed cardiotoxicity, dermonecrosis, myotoxicity, haemolysis, neurotoxicity, hepatotoxicity and lethality in experimental animals.

Mawia benovici (Piraino, Aglieri, Seorrano & Boero, 2014) ( ¼ Pelagio benoviei)

Common name (s): Golden jellyfish Global distribution: Gulf of Venice, Adriatic Sea, Mediterranean Sea. Ecology: It lives in coast line to offshore at 20–25 m depths. Biology Description: Exumbrella of this species is yellow ochre in colour and is homo- geneously covered by prominent cnidocyst warts of various shapes. Its 16 marginal lappets are rectangular, with rounded corners. There are eight adradial, hollow, white and transparent tentacles which are up to three times the diameter of umbrella in length. Its eight marginal sensory organs lack ocelli. Each of such sensory organs is located in a shallow pit formed by ectodermal outgrowth of the umbrellar margin. Stomach is without gastric septa. There are four interradial, elongated milky white, ribbon-like gonochoric gonads. Manubrium is whitish, transparent and is 1.5 times the diameter of umbrella in length. Food and feeding: Its food and feeding habit is not as it is a new species. However, it may be a carnivore eating fish eggs and larvae, as well as tiny crustaceans. Envenomation: The long tentacles of this species and its affiliation to other venomous members of the Pelagiidae family suggest that it can inflict painful stings to human beings (Anon. http://jellyrisk.com/media/cms_page_media/115/printed% 20manual%20-%20English%20version.compressed.pdf). Montgomery et al. (2016) reported that the sting severity of this species is medium. 110 4 Biology and Ecology of the Venomous Marine True Jellyfish (Class Scyphozoa)

Remarks: Researchers are just starting to get to know about this new species and much work remains to be done.

Pelagia noctiluca (Forsskal, 1775)

Image credit: Wikimedia Commons Common name (s): Mauve stinger, purple-striped jellyfish Global distribution: It is widely distributed in all warm and temperate waters of the world’s oceans, including the Mediterranean Sea, Red Sea and Atlantic Ocean. It is also found in the Pacific Ocean areas such as Hawaii, southern California and Mexico. Ecology: This is typically an offshore species, although sometimes it is washed near the coastlines and may be stranded in great numbers on beaches. Biology Description: Umbrella of this species is bell-shaped or hemispherical, and its colour can range from purple to brownish red. It has a frilled edge on the bell, with eight thin, stinging tentacles and four lobes hanging down from the mouth, called oral arms. Its umbrella edge is divided into eight lobes, where sense organs such as light receptors and odour pits are located. Tentacles are very elastic. It is a bioluminescent species, i.e. it has the ability to produce light. Light is emitted in the form of flashes when the medusa is stimulated by turbulence created by waves or by a ship’s motion. This flashing is only of relatively short duration and gradually fades. 4.13 Family Pelagiidae 111

Food and feeding: It is carnivorous like other cnidarians and preys mainly on zooplankton, small fish, crustaceans, other jellyfish and eggs. It captures its prey with tentacles armed with cnidocytes, each of which contains a nematocyst. Nematocysts have barbed filaments to trap their prey and toxins to stun them. They can even pierce the shell of a crab with their barbs. Life cycle: The adults of this species with separate sexes reproduce sexually by releasing gametes from gonads located near the centre of the body. The ova and sperm are released through the mouth of the jellyfish and fertilize externally. Each fertilized egg forms a planula that swims with external cilia. Planula may be widely dispersed by oceanic currents. Unlike other species which have a bottom-dwelling polyp stage, the planulae of this species develop directly into ephyrae, young medusae. The ephyra quickly grows into an adult medusa (Leverenz 2000). Uses: One possible use of the fluorescent protein of this species is as a genetic marker to detect protein movement or gene expression in research in developmental, environmental and medical biology (Manning 1997). Economic loss: The level of “mortalities” due to this species is believed to be the worst of farmed fish on the island of Ireland since 2008 when some 250,000 salmon were killed in Northern Ireland. In November 2007, a 10-square-mile swarm of this specie wiped out a salmon farm with 100,000 fish also in the North, causing £1 million worth of damage (O’Sullivan 2017). Envenomation: The sting of this species is venomous to humans, but normally only causes a whip-like scar across the body. In rare cases of allergic reactions, life- threatening conditions like anaphylactic shock can occur (Anon. https:// animaldiversity.org/accounts/Pelagia_noctiluca/). Morabito et al. (2017) reported that this species is the most venomous and possesses a venom with haemolytic and cytolytic activity. Anon. (http://www.cmas.org/news/watch-out-for-the-gelatinous-organisms-of- the-eastern-mediterranean) reported that this species is considered as the most venomous, severe stinging jellyfish in the Mediterranean. The tentacles, oral arms, exumbrella and gastric pouches are covered in nematocysts, which means that all the body parts can sting. The local symptoms of its sting include erythema, oedema and vesicles as well as persisting pain in the stung skin. It takes 1–2 weeks for the pain to completely disappear. Hyper pigmentation may also occur on skin. Systemic symptoms of its sting include bronchospasm, pruritus, dyspnoea, numbness, nausea, vomiting, low blood pressure, diarrhoea and shock. Mariottini (2014), Montgomery et al. (2016) and Remigante et al. (2018) reported that the sting severity of this species is high and its crude venom isolated from the nematocysts from the oral arms showed haemolytic activity on human RBCs. 112 4 Biology and Ecology of the Venomous Marine True Jellyfish (Class Scyphozoa)

Sanderia malayensis Goette, 1886

Common name (s): Amakusa jellyfish. Global distribution: This species is native to the tropical Indo-Pacific region. Its range includes Red Sea and Suez Canal, Pakistan, Malaysia, Philippines and Japan. Ecology: It is a coastal, planktonic species. Biology Description: Medusa phase of this species is distinguished from other related species by having 32 marginal lappets at the edge of the transparent bell, and 16 tentacles alternating with 16 rhopalia. Edge of the bell has a short vertical “skirt”, about as wide as one-sixth of the bell. Stomach has four heart-shaped radial pouches each edged with up to 40 finger-like gonadal papillae. Bell is topped by a number of warts laden with nematocytes. This jellyfish is transparent and may be yellowish or tinged violet. Sometimes there are radiating rows of reddish spots on the bell or on the mouth arms. Diameter of the bell may vary from 3 to 13 cm. Its marginal tentacles can be 29 cm long with the frilled mouth arms which are 16 cm long. Life cycle: This species has a complex life cycle with a number of types of asexual reproduction. New polyps can bud off existing polyps, with a moveable stolon. Strobilation of the polyp may occur with the formation of ephyrae which separate from the mother polyp. Sexual reproduction can also occur with eggs liberated into the sea by the adult medusa. When fertilized, these develop into a free-living planula, then to a scyphistoma, to a strobila and lastly to a free-living young medusa. Envenomation: This venomous species has caused injuries to humans. One report from the Persian Gulf near Kuwait stated that it caused severe stings with necrosis of the skin. Other reports describe it as causing “peripheral vasospasm” and “peripheral tissue necrosis” (Blaxter et al. 1984; Burnett et al. 1996; Anon. https://en.wikipedia. org/wiki/Sanderia_malayensis). 4.14 Family Periphyllidae 113

4.14 Family Periphyllidae

Periphylla periphylla (Peron & Lesueur, 1810)

Common name (s): Helmet jellyfish, red-coloured jellyfish Global distribution: It is found in every ocean of the world, as well as in the Norwegian fjords and in the Mediterranean Sea. Ecology: This jellyfish is found in depths up to 7000 m and is adapted to its dark environment, deep sea. Biology Description: Animals of this species with bell-shaped body can be up to 20 cm long, and their bodies, or central domes, have a diameter of up to 35 cm. Its coronal groove, located on the lower portion of the bell, provides flexibility for movement. This coronal groove divides the aboral surface into the central dome and the peripheral zone, which contains radial thickenings called pedalia and marginal lappets that contain some sense organs. It has 12 stiff tentacles. These animals have dark red and/or brown stomachs. Mouth is very simple and is located on the manubrium. Externally, males and females of this species are similar. It is a bioluminescent species. Food and feeding: These medusa feed mainly on calanoid copepods, ostracods and large euphausiids. At night this jellyfish leaves the depths and swims up towards its food. With full stomach it turns from the surface back to the depths. Life cycle: The medusae of this species do not go through a polyp stage, thus presenting a “holopelagic” life cycle. The fertilized eggs thrown by these medusae in 114 4 Biology and Ecology of the Venomous Marine True Jellyfish (Class Scyphozoa) open water develop directly into medusae, whose development rests entirely upon the egg’s high yolk supply. The ephyra stage that is common among other jellyfish is not observed in this species. Envenomation: Montgomery et al. (2016) and Mariottini (2014) reported that the sting severity of this species is mild and its crude venom has shown haemolytic activity.

4.15 Family Rhizostomatidae

Nemopilema nomurai Kishinouye, 1922

Common name (s): Nomura’s jellyfish. Global distribution: Subtropical north-west Pacific: endemic to the East Asian Marginal Seas; between China and Japan, primarily centralized in the Yellow Sea and East China Sea. Ecology: It is residing in coastal waters. Explosive blooms of this species have been on the increase. Biology Description: It is one of the largest jellyfish species and is growing up to 2 m in diameter and weighing up to 200 kg (Kawahara and Dawson 2007). Little is known about the biology and ecology of this species. Food and feeding: This species feeds mostly on zooplankton in its earlier stages and on larger fish as it grows large. Predators: Its predators consist of swordfish, tuna, sunfish, leatherback turtles and humans. Life cycle: In the sexual reproduction of this species, fertilized egg develops into a planula larva after 1 day. Planula swims for 4–8 days until it becomes a translucent, whitish and dome-shaped scyphistoma and settles at the bottom. Fully developed scyphistoma appears after 10–20 days of settlement. This species also exhibits asexual reproduction by means of podocyst formation (as many as 18 podocysts 4.15 Family Rhizostomatidae 115 on a single original scyphistoma within 7 days to 3 months). Scyphistoma colony develops from podocyst of original scyphistoma within 6 months. Fully developed scyphistoma develops into a strobila after a day and becomes a liberated ephyra with 5–7 days. A fully developed metaphyra appears within 30 days of post-liberation and becomes a young medusa within 40–50 days of post-liberation. Furthermore, ephyrae are released into the plankton during early summer. After subsequent sexual reproduction, the medusae die during winter. The life span of the medusae is less than a year. Edible values: It is edible but not considered high quality. Dairy produces a vanilla and jellyfish ice cream using this jellyfish species. Ecological importance: Occurrence of bloom of this species has threatened the fisheries in Japan since early 2000s. Envenomation: The venom of this species possesses proteins and enzymatic components such as metalloproteinase and phospholipase A2s. Victims of stings from this jellyfish may present symptoms of itching, swelling, acute pain, local erythrosis and inflammation; and in severe cases, the envenomations can cause death (Anon. https://en.wikipedia.org/wiki/Nomura%27s_jellyfish). This species was responsible for most severe or fatal cases of jellyfish stings in Chinese sea. Besides cutaneous symptoms, the venom extract of this species showed selective toxicity on cardiac tissue (Dong et al. 2010). Anon. (http://thescyphozoan.ucmerced.edu/Org/JotQ/JotQ_07Aug.html) reported that the stings of this species caused predominantly non-lethal effects although a few deaths have been reported from China. When stung by this species, there is at first a very intense pain with strong burning sensation, then the site of the sting becomes reddened and small blisters form on the surface of the skin. The symptoms subside after about half an hour. Mariottini (2014) reported on the haemolytic activity of the venom of this species. Remigante et al. (2018) reported that the nematocyst venom of this species showed PLA2/PLA2-like catalytic activity. Further, this venom also showed the presence of main proteins such as matrix metalloproteinase-14 and astacin-like metalloprotease; and predominant metalloproteinase enzymatic activity. Further- more, hyaluronidases and L-amino acid oxidases have also been detected in the nematocyst venom of this species. Seyedian et al. (2007) reported that the venom of this species produced cardiovascular effects such as hypotension, bradycardia, transient decrease in blood pressure and contraction in the rat isolated atria. 116 4 Biology and Ecology of the Venomous Marine True Jellyfish (Class Scyphozoa)

Rhizostoma luteum (Quoy & Gaimard, 1827)

Image credit: Shutterstock Common name (s): None Global distribution: Tropical eastern Atlantic and the Mediterranean: Portugal, Gibraltar, Angola, Mauritania and West Africa. Ecology: It lives in coastal waters. It is an imposing animal and is mostly occurring as single individuals. It is moving with slow and powerful pulsations. It can become microcosms that are used by other organisms. While it provides a shelter for juvenile fish, its oral arms serve as refuge for small crabs. Biology Description: It is the largest jellyfish in the Alboran Sea. Umbrella can reach a diameter of 60 cm and weight more than 20 kg. Colour of the body is white. Manubrium is large and it looks like a white cauliflower. It has many small mouths. Oral arms have a yellow-grey-bluish colouring in the parts furthest away from the umbrella, with eight long (up to 2 m) terminal appendages of a dark brown purple colour. Life cycle: The life cycle of this species resembles that of its congeners, with the distinction that it has the unique features of being a brooding species (internal fertilization with subsequent release of planulae). Further, a monodisc strobilation appears in this species. Envenomation: Its sting is not very painful, but they can cause mild to severe rashes if touched with insistence (Anon. http://jellyfishresearchsouthspain. moonfruit.com/especies-species/4588865667). Montgomery et al. (2016) reported that the sting severity of this species is medium. 4.15 Family Rhizostomatidae 117

Rhizostoma pulmo (Linnaeus, 1758)

Image credit: Wikimedia Commons Common name (s): Barrel jellyfish, dustbin-lid jellyfish, frilly mouthed jellyfish, Global distribution: Subtropical north-east Atlantic, and in the Adriatic, Mediter ranean Sea, Black Sea and Sea of Azov; southern Atlantic: off the western South African coast and into False Bay; Irish Sea. Ecology: This species swims in the vicinity of surface in pelagic zone and also in littoral zone. Biology Description: Umbrella of this species is hemispherical and translucent. Exumbrella surface is finely granular; jelly is thick; and central portion is stiff, thinner and flexible in outer third. There are 8–12 velar marginal lappets per octant and marginal tentacles are absent. Eight rhopalia are present. Subumbrellar musculature is in eight distinct peripheral muscle fields. Stomach is occupying central third of bell. Manubrium is short, massive and translucent. Its eight oral arms are inverted Y-shaped in section, supporting two long, massive, outwardly directed blades also bearing numerous mouthlets. Oral arms are without lateral clubs and filaments, and each arm is with a large, translucent terminal club. There are four gonads and each of them is a much convoluted lobe. In older animals surface of gonad is bearing grooves which are extending to its edge. Umbrella diameter reaches up to 90 cm. Surface of umbrella is pale grey to colourless but may also be pale milk white, opalescent and rose red. Gonads are largely white. 118 4 Biology and Ecology of the Venomous Marine True Jellyfish (Class Scyphozoa)

Marginal lappets are narrowly edged with ultramarine blue, violet or brown line of dense colour. Rhopalar lappets are colourless. Canals in the terminal clubs of the oral arms may be bright blue, yellowish brown, pink, deep purple-brown or colourless. Maturing gonads are tinged brown to reddish brown or blue. Predators: It is a favourite food of the leatherback turtle. Life cycle: In sexual reproduction of this species, egg is laid by the adult medusa which later develops into a free-living planula, then to a scyphistoma to a strobila and lastly to a free-living young medusa. Association: Specimens of this species are found wrapped of alevins (a newly spawned salmon or trout still carrying the yolk) swarm of various species. In this association only alevins would beneﬁt. Envenomation: It is rather not very irritant as the cnidocytes are slightly poisonous and do not transpierce the human skin. Thus there is thus no risk of lesion (Anon. https://en.wikipedia.org/wiki/Rhizostoma_pulmo). Turk (1999) reported that this species may inﬂict a painful sting and one should be cautious in handling it with bare hands. Mariottini (2014) reported that a cytolysin, viz. rhizolysin, isolated from the nematocysts of this species induced haemolysis on human and rat RBCs. Montgomery et al. (2016) reported that the sting severity of the venom of this species is mild.

Rhopilema esculentum Kishinouye, 1891

Image credit: Flickr Common name (s): Flame jellyfish Global distribution: Tropical north-west Pacific: China and Japan. Ecology: It drifts with the currents and is found near the surface in calm weather. It is swept inshore by the rising tide and drifts back out as the tide falls. Biology Description: Bell of this species which is 45 cm wide and 33 cm high is rigid, tough and thick with a smooth surface. It is usually suffused with red. Exumbrella is smooth. In each 14–20 oval velar lappets, there are numerous radial grooves. Mouth 4.15 Family Rhizostomatidae 119 arms have no definite terminal clubs, but numerous filamentous and large fusiform appendages are seen between the mouths. Edible value: This jellyfish is a popular item of food in China and other southern and eastern Asian countries. It can be eaten raw as a salad and has a crisp texture. Aquaculture value: The commercial aquaculture this species has expanded greatly in China. Envenomation: This species has been virulent to humans. It produced significant pruritus. The lesions of this jellyfish species are characteristic and common in workers harvesting medusa (Kawahara et al. 2006). Mariottini (2014) reported on the haemolytic activity of the venom of this species. Remigante et al. (2018) reported that the venom extract of the oral arms of this species showed the presence of metalloproteinases and associated gelatinolytic, caseinolytic and fibrinolytic activities; and PLA2/PLA2-like catalytic activity.

Rhopilema hispidum (Vanhoffen, 1888)

Common name (s): Not designated Global distribution: Tropical Indo-West Pacific: Hong Kong, Malay Archipelago, Philippines and India. Ecology: It is a pelagic species. Biology Description: Bell of this species ranges from 120 to 650 mm in diameter. Exumbrella is whitish in colour and rough with minute, colourless, blunt warts giving the exumbrellar surface a granulated appearance. Larger, brown, conical, pointed warts are abundant near the margin of the exumbrella and velar lappets. These warts are becoming gradually sparse and less pronounced in size towards the bell centre. There are eight oblong to round velar lappets per octant and are connected by thin membranous webs. Rhopalar lappets are pointed. Distal exumbrellar surface of both velar and rhopalar lappets have some minute irregular vertical stripes. Mouth arms are eight, J-shaped and three-winged and are fused in 120 4 Biology and Ecology of the Venomous Marine True Jellyfish (Class Scyphozoa) the proximal half of their length. Each wing is bearing numerous frilled mouths and small club-shaped appendages. A large club-shaped appendage is present at the point of contact of the three wings. Four long, whip-like appendages are arising from the oral side of the fused part of the mouth arms. Food value: This is an edible jellyfish. Association: It is the host to a few fishes (carangid, eel larvae, ponyfish), a shrimp, a crab, a copepod and a flatworm. This association is presumed to be commensalism. Envenomation: This jellyfish is virulent to humans. It caused a persistent eruption which is characteristic and common in workers harvesting medusa (Kawahara et al. 2006).

Rhopilema nomadica Galil, 1990

Common name (s): Nomad jellyfish Global distribution: Tropical warm waters of the Indian and Pacific Oceans; eastern Mediterranean off the coast of Israel, Turkey and in the Aegean Sea off the coast of Greece. Ecology: It is a neritic, epipelagic species. It can survive from anywhere from 16 Cto31C. Its swarms have been recorded at a distance of 2–4 km off shore. Occasionally it is swept nearer shore and into the intertidal zone. Biology Description: it is a medium-sized rhizostomid medusa. It has a nearly hemispherical umbrella, which is thickest centrally and is thinning gradually towards margin. Exumbrella is minutely granulate and granules fewer and blunter near margin. Margin of umbrella is divided into 64 rounded velar lappets. Ocular lappets are small and lanceolate. Subumbrellar circular muscles are well developed. Arm disc is prismatic and is about one-third of bell diameter; and oral pillars are quadrate. Distal 4.15 Family Rhizostomatidae 121 corners of oral pillars are prominently tuberculate. There are eight pairs of large, deeply bowed scapulets arise from adradial sides of arm disc. Its eight adradial mouth arms are stout, smooth and are fused to midlength. Lower part of mouth arm is divided into two triangular flaps, and each flap is distally tripartite and terminating in claw-like digitate processes. Ventrally, mouth arms bear numerous frilled mouths and long filaments. Lowermost end is bearing a vermicular appendage terminating in a thin filament. Stomach cavity is nearly octagonal. Gastrovascular system is consisting of four perradial, four interradial and eight adradial canals. Four principal canals extend from lower part of stomach to radii entering each scapulet and mouth arm, then branching to numerous minute canals leading to mouths. Colour of this medusa in life is icy blue. It can reach up to 100 cm umbrella diameter. Food and feeding: It is a planktotrophic species (feeding on plankton). Predators: It is eaten by fish and marine turtles. Life cycle: It has a two-stage life cycle consisting of the conspicuous, large, sexually reproducing swimming medusa stage and a benthic polyp stage (scyphistoma). Fertilization is external and planulae are formed within hours. Settlement occurs within 3–4 days, and polyps are developed within 3 weeks. Asexual reproduction occurs mostly through podocyst formation. Polyps produce podocysts by growing stolons from the base of the disk. Polyps are developed into polydisc strobilae within 45 days. The strobilation process is complete in 7 days; and 5–6 ephyrae are formed on each strobila. Mature polyps may strobilate repeatedly. The development from the newly released ephyra (1.5–2 mm in diameter) to the young medusa (7–10 mm in diameter) may be completed within a period of 2 months. Association: The juveniles of the shrimp scad, Alepes djedaba, are commonly found in association with this species. It is possible that the great increase in the carangid’s abundance in the 1980s owes to the presence of R. nomadica sheltering juveniles. Envenomation: This species can cause very painful injuries to humans since it has vermicular filaments, which are covered in venomous stinging cells, in the mouth arms. R. nomadica had caused the largest numbers of envenomisations along the southern Levant coast (Anon. https://en.wikipedia.org/wiki/Rhopilema_nomadica). This species has negative consequences on human health, tourism and fishing activities. Many people swimming on the beaches have been stung and sought for a medical treatment. Local fishermen claim a decrease in catch from their stationary nets (e.g. gill net) as they clog the nets and make them heavy (Anon. http://www. cmas.org/news/watch-out-for-the-gelatinous-organisms-of-the-eastern- mediterranean). R. nomadica’s toxin-loaded nematocysts cause envenomation, usually expressed as immediate appearance of redness, burning sensation and papulovesicular and urticaria-like swelling of the affected skin, causing intensive pain and very itchy skin. The symptoms, in severe cases, may last several weeks (https://www.cabi.org/ isc/datasheet/108185). Partially purified venom from this species elicited unstable haemolytic activity against human, rabbit, sheep and guinea-pig RBCs (Mariottini 2014). 122 4 Biology and Ecology of the Venomous Marine True Jellyfish (Class Scyphozoa)

Montgomery et al. (2016) reported that the sting severity of this species is medium. Remigante et al. (2018) reported on the occurrence of a polypeptide toxin with sequence similarity to PLA2 (phospholipase A2, lipase) from the tentacles of this species (Remigante et al. 2018).

Rhopilema rhopalophora Haeckel, 1880

Common name (s): Not designated Global distribution: Tropical Indo-West Paciﬁc: Madagascar and China; Indian Ocean. Ecology: It is a pelagic species Biology Description: Bell of this species is 10 cm in width and 5 cm in height. Exumbrella is smooth, and is very thin. In each octant, there are 14–16 roundish, ﬂat velar lappets. Subgenital papillae are absent. Scapulets are small. Manubrium is extraor- dinarily short; mouth arms are about 2.5 m long (proximal portion 0.3 m, distal portion 1.2 m and terminal club 1–1.2 m long). A very few small clubs are seen on mouth arms. Filaments which are present only on scapulets are faintly developed. Ring canal is poorly developed. Envenomation: Although this species is venomous, there are no reports about its sting severity (Montgomery et al. 2016). 4.16 Family Stomolophidae 123

4.16 Family Stomolophidae

Stomolophus meleagris (Agassiz, 1860)

Image credit: Wikipedia Common name (s): Cabbagehead jellyfish, cannonball jellyfish Global distribution: Cannonballs are prominent from North America’s eastern seaboard all the way to Brazil and are also found in parts of the Pacific. Pacific Ocean (South China Sea to Sea of Japan, and California to Ecuador) and the mid-west; Atlantic Ocean (New England to Brazil); common on the south- eastern coast of the United States, including the Gulf Coast. Ecology: It is found within saline and estuarine waters by the shoreline. The waters they inhabit are usually around 23.1 C and on average the water salinity is 33.8 ppt. Biology Description: It is a small jellyfish with a maximum bell width of 25 cm. Some have been found up to 25 cm in width. Mass ranged in one study from 143 to 1378 g. This jellyfish looks like a thick hemispherical bell and can have several different colour schemes, including milky blue or yellow, with or without a border of brown 124 4 Biology and Ecology of the Venomous Marine True Jellyfish (Class Scyphozoa) pigment. It has 16 short, forked fused orals arms instead of the normal tentacles. It also has secondary mouth folds (scapulets) covered with mucus. Food and feeding: Cannonballs eat mainly zooplankton including veligers. Predators: One of the main predators of cannonball jellyfish is the endangered species leatherback sea turtle. Cannonball jellyfish are also commercially harvested as food for humans. Life cycle: It can reproduce both sexually and asexually. During sexual reproduction, cannonballs shoot sperm out of their mouth. The sperm are then caught by another cannonball through the mouth and fertilization takes place. The embryo begins to develop in specialized pouches found on the arms around the mouth. After about 5 h, the larvae fall to the bottom and attach a hard substratum where they develop into polyps. After several days, the polyp will detach and become a swimming ephyra and will eventually turn into an adult jellyfish. Association: They have a symbiotic relationship with the portly spider crab which feeds on the prey captured by the cannonball and also on the medusae of the jellyfish. Envenomation: Although cannonballs do not commonly sting humans, they do have toxins which can cause cardiac problems in humans. This toxin causes irregular heart rhythms and problems in the myocardial conduction pathways. The toxin of this species is also harmful to the eyes; and contact with a nematocyst can be very painful, followed by redness and swelling. However, cannonball jellyfish are mostly harmless to humans. Contact with them may cause the skin to itch slightly, or minor eye irritation (Anon. https://en.wikipedia.org/wiki/Cannonball_jellyfish). Mariottini (2014) reported that the nematocyst venom of this species showed the presence of haemolytic protein SmTX which induced strong haemolytic effects in human RBCs. Frazão and Antunes (2016) reported on the presence toxins such as SmP90, C-type lectin, PLA2, Kv+ toxin, haemolysin and metalloprotease. Remigante et al. (2018) reported that the venom of this species contained PLA2 (phospholipase A2) (which is responsible for the development of pain, inflammation and cell lysis consequent to the envenomation) and certain proteins defined as “K+ channels inhibitors” from this species. 4.17 Family Ulmaridae 125

4.17 Family Ulmaridae

Aurelia aurita (Linnaeus, 1758)

Image credit: shutterstock Common name (s): Common jellyfish, moon jellyfish, moon jelly or saucer jelly Global distribution: It is found mostly in warm and tropical waters worldwide; common along the eastern Atlantic coast of Northern Europe and the western Atlantic coast of North America in New England and Eastern Canada. Ecology: It is an inshore species, but it can also be found in estuaries (with salinity as low as 0.6%) and harbours. It is capable of only limited motion, and drifts with the current, even when swimming. These jellyfish are capable of withstanding temperatures as low as À6 C and as high as 31 C. Biology Description: These jellyfish are transparent and their umbrella (bell) is flat and flexible with eight simple marginal lobes. There are few hundred to more than 1000 small filiform marginal tentacles which are, arising nearly at bell edge. From their stomach lead 16 unbranched adradial canals ((eight perradial and eight interradial). Four unbranched oral arms are found dangling down. Gonads are invaginated, with external subgenital pits, appearing as four horseshoe-shaped ribbons in the gastric cavity, conspicuous due to their colour and transparency of bell (Santhanam and Srinivasan 1994). Bell diameter of these jellyfish may range from 25 to 40 cm (Santhanam and Srinivasan 1994). Food and feeding: These jellyfish feed on zooplankton and are carnivorous. They feed primarily on molluscs, rotifers, crustaceans, nematodes, diatoms, fish larvae and tunicate larvae. When the tentacles brush against the prey, their sting cells with powerful toxins render them inactive. The inactive prey is then collected primarily 126 4 Biology and Ecology of the Venomous Marine True Jellyfish (Class Scyphozoa) on the surface of the jellyfish, where they get entangled in the mucus. Further, by flagellar action, food is passed through the mouth, along the eight canals inside the jellyfish’s body. These canals run into the stomach and bring the food to the stomach via the ring canal, where it is broken down by digestive enzymes. Predator: The known predator of this jellyfish is sea turtle. Reproduction: These jellyfish are either male or female. The young larval stage, a planula, has small ciliated cells and after swimming freely in the plankton for a day or more, settles on a suitable substrate, where it metamorphoses into a special type of polyp called a “scyphistoma”, which divides by strobilation into small ephyrae that swim off to grow up as medusae (Santhanam et al. 2015). Envenomation: The moon jellyfish is considered to be one of the seven most deadliest, most poisonous Jellyfish in the world (Kye 2014). The net of tentacles present in the lower part of the body of jellyfish are studded with scores of poisonous sting cells called cnidocytes or nematocysts, which are capable of injecting poison. The moment the tentacles brush against a prey, the numerous sting cells explode, thereby launching barbed stingers and poison into the prey’s body. Segura-Puertas et al. (2002) demonstrated that A. aurita can be venomous to humans and elicit localized skin eruptions. It was also reported that 136 persons were stung by A. aurita in the coast of Shandong province (China), in which 18 patients showed severe clinical symptoms (Dong et al. 2010). Simmons et al. (2015) reported that the contact with this jellyfish led to intense stinging pain followed by subsequent pruritus and the formation of urticaria after a few minutes that persisted for several hours. Remigante et al. (2018) reported that these jellyfish which are abundant in the Mediterranean Sea may cause, in addition to dermatonecrosis, systemic symptoms such as fever, dyspnoea and muscle weakness. Segura-Puertas et al. (2002) reported that the venom of this jellyfish has haemolytic, proteolytic and mytotoxic activities. The crude venom and its partially purified fractions have been reported to produce haemolysis, cytotoxicity, dermonecrosis and lethality. Further, the tentacle venom extract of this species showed significant neurotoxic effects and associated tetanic reactions, flaccid paralysis and death when injected into crabs (Ponce et al. 2013). Remigante et al. (2018) reported on the presence of metalloproteinases in the venom of this species. Its C-type lectins exhibited pro/anti-coagulant and pro/anti- thrombotic activities and its tentacle venom extract potently inhibited ACh-elicited currents mediated by both vertebrate foetal and adult muscle nicotinic acetylcholine receptor (nAChR) subtypes. Further, the venom of this species also showed the presence of five proteins similar to the CaTX family of haemolysins, pore-forming toxins TX1 and TX2 and ATPase-like (Av120) proteins. Remigante et al. (2018) also reported on the high PLA2 (phospholipase A2) catalytic activity of the venom of this species. 4.17 Family Ulmaridae 127

Mariottini (2014) reported that the venom of this species showed haemolytic activity. Frazão and Antunes (2016) reported on the presence of the toxin aurelin from this species. Segura-Puertas et al. (2002) reported on the abdominal region sting of this species.

Deepstaria enigmatica Russell, 1967

Common name (s): None Global distribution: It is found in Antarctic and near-Antarctic seas; also in waters near the United Kingdom. Ecology: It is found at dark depths (600–1750 m) of the ocean. It is so fragile and it just ﬂoats in the midwater. Biology Description: Bell of this species is remarkably thin, broad and delicate and is up to about 60 cm diameter. It resembles a translucent, undulating sheet or lava lamp as the animal moves. Mesoglea is 1–2 cm thick and is tapering towards edge. There are 8–20 rhopalia which increase during growth, and rhopalar lappets are rectangular with circular ends. Marginal tentacles are absent. Stomach is small, about 1/6 of total bell diameter, circular and is protruding beneath subumbrella as short, thick-walled manubrial tube. Its 4–5 oral arms are narrow and elongate. Gastrovascular canals are ﬁne, somewhat irregular-edged and are forming reticulate network across most of 128 4 Biology and Ecology of the Venomous Marine True Jellyfish (Class Scyphozoa) bell. There are 8–20 radial canals. Gonads (4–5) are short-stalked and lobed and are attached near the base of oral arms. Though most specimens reported are colourless, specimens with deep brown exumbrella have also been reported. Food and feeding: It is an ambush predator that uses its entire bell membrane to catch upward-moving prey, closing around it like a bag. Envenomation: Montgomery et al. (2016) reported that the sting severity of this venomous species is mild.

Deepstaria reticulum Larson, Madin, and Harbinson, 1988

Common name (s): Not designated Global distribution: Tropical eastern central Pacific and western central Atlantic: USA and Bermuda. Ecology: It is a pelagic species occurring at depths of 600–915 m. Biology Description: It has a wide, fan-like bell that is often a deep purple colour. Bell is spread wide, like a thin, translucent bed sheet. Under the bell, there is a small cluster of tentacles. Food and feeding: It is a suspension feeder and is free-floating in the water column in wait for unsuspecting prey. Envenomation: It is a venomous species and under tits bell, there is a small cluster of tentacles, loaded with stinging, venomous barbs like any other jellyfish (Anon. https://en.wikipedia.org/wiki/Deepstaria_reticulum). 4.17 Family Ulmaridae 129

Discomedusa lobata Claus, 1877

Common name (s): None Global distribution: Subtropical north-east Atlantic and the Mediterranean: France, English Channel and West Africa. Ecology: It is a pelagic species Biology Description: Umbrella of this species is quite flat and disc-shaped with a width of 150 mm. Jelly is moderately thick and clear. It has 8–9 rhopalia, 8–40 tentacles, 32–48 lappets and 8 perradial and interradial canals which are branched and usually anastomosing with the 8 simple adradial canals. Mouth arms are thick and broad, but their margins are more curtain-like, and more folded, with numerous tentacular filaments. Stomach is circular, wide and is occupying central 1/2 of disc. Its four gonads are in much-folded ribbon lying near stomach periphery. They are sac-like when mature and are projecting from the floor of subumbrella. Numerous dark brown pigment spots are present on the 16 radial exumbrellar streaks. Nematocyst warts are arranged in star pattern aligned with ridges in underlying mesoglea. 130 4 Biology and Ecology of the Venomous Marine True Jellyfish (Class Scyphozoa)

Envenomation: it is generally considered capable of inﬂicting painful stings on the same par as the much more common mauve stinger (Anon. https://www. timesofmalta.com/articles/view/20130912/local/two-new-jellyﬁsh-species- recorded-in-maltese-waters.485855). Montgomery et al. (2016) reported that the sting severity of this venomous species is mild.

Phacellophora camtschatica Brandt, 1835

Common name (s): Fried-egg Jellyfish, egg yolk jellyfish Global distribution: These are temperate water animals that live from the Gulf of Alaska to Chile on the eastern Pacific coast, as well as within the Atlantic and Mediterranean. Ecology: It is a coastal, pelagic species. Generally it hangs motionless in the water with its tentacles trailing behind. Biology Description: Bell of this species is up to 60 cm in diameter and is with 16 clusters of tentacles of 3–6 m long. There are 16 lappets and 16 rhopalia. Oral arms are relatively short and massively folded. Its delightful yolk-like middle of the medusa is gonadal tissue which is usually yellow. However, the colour can change with the diet of the animal. Small individuals are often colourless or milky white. Food and feeding: These glorious gelatinous animals survive by eating other gelatinous zooplankton (like medusa) which become ensnared in the tentacles. 4.17 Family Ulmaridae 131

Life cycle: It alternates between a benthic stage attached to rocks and piers that reproduces asexually and the planktonic stage that reproduces sexually in the water column. Envenomation: Montgomery et al. (2016) stated that the sting severity of this venomous species is mild. Anon. (https://gelatinoussting.com/2018/04/11/species-spotlight-egg-yolk- jellies/) stated that as of now, its venom has not been characterized. Though unpleasant, its sting is not truly dangerous to humans, which makes some inherent sense.

Poralia rufescens Vanhoffen, 1902

Common name (s): None Global distribution: Subtropical Atlantic: Azores Island Bermuda, USA and Canada; also in cold Southern Ocean around Antarctica. Ecology: It is a deep-water, pelagic species. Biology Description: Disc of this species which is 25 cm wide is flat with short, vertical peripheral skirt. Jelly is thin and in life, disc is flexing from flat, through hemispherical to fully spherical (with opposite sides of margin meeting) in overall shape. Skirt is supported by strong ribs with equal intervening gaps. Exumbrellar rhopalial pits are somewhat conspicuous and are situated near upper margin of skirt. Rhopalium is short and stubby. Rhopalial lappets are long, pointed, straight-sided and without gap 132 4 Biology and Ecology of the Venomous Marine True Jellyfish (Class Scyphozoa) between. Marginal tentacles numbering 24 are alternating in ones and twos with the 16 rhopalial lappets. Marginal tentacles are of the same length as disc diameter and are arising from exumbrella surface. Its eight mouth arms are arranged in pairs and are tapering gradually to blunt point. Their length in life is about 1/2 bell diameter. Stomach is circular, occupying central 1/3 of disc. Radial canals numbering 48 (depending on stage of growth) are wide, and irregular, leading to wide peripheral ring canal. Its 16 per-, inter- and adradial canals are continuing beyond ring canal for short distance and are then forking on either side of each rhopalium. Gonads (8) are arranged in (near) continuous ring around the periphery of the stomach, and the diameter of gonad ring is approximately 1/3 of disc diameter. Ground colour of epidermis of disc is pale orange and translucent; radial canals are whitish; mouth arms are pale lilac and marginal tentacles are colourless. Envenomation: Montgomery et al. (2016) reported that the sting severity of this venomous species is mild. Biology and Ecology of the Venomous Marine Box Jellyfish (Class Cubozoa) 5

5.1 Family Alatinidae

Alatina alata (Reynaud, 1830) ( ¼ Carybdea alata)

Common name (s): Sea wasp

# Springer Nature Singapore Pte Ltd. 2020 133 R. Santhanam, Biology and Ecology of Venomous Marine Cnidarians, https://doi.org/10.1007/978-981-15-1603-0_5 134 5 Biology and Ecology of the Venomous Marine Box Jellyfish (Class Cubozoa)

Global distribution: Subtropical; Circumtropical; ranges across the Pacific and Atlantic and Indian Ocean; also Arabian Sea along the beaches of Pakistan. Ecology: This pelagic species is found in shallow waters near shore, and also occurs offshore in deeper waters, in a depth range of 55–2282 m. Biology Description: It has a tall narrow bell, flared at base and is tapering into truncated pyramid at apex. It is also transparent and very hyaline (glassy). Species of the Pacific (not including areas near Hawaii) are often very large up to 300 mm long and up to 150 mm wide. Atlantic specimens are 250 mm long and 130 mm wide. There are four crescentic gastric phacellae at interradial corners of stomach; three simple to palmate branching velarial canals per octant, each with a velarial lappet bearing a row of three to four nematocyst warts; and four long wing-like pedalia, each with a pink tentacle. Cnidome is consisting of heterotrichous microbasic p-euryteles and small birhopaloids in tentacles, and large isorhizas in nematocysts warts. It has a life span of only 1 year. Food and feeding: It preys on plankton, larval fish of the species Stegastes planifrons, caridean shrimps and polychaetes which are easily grasped by the tentacles. Predators: Batfish, butterfish, crabs and sea turtles like the green turtle are the predators of this species. Association: Live medusae of this species collected from Bonaire had hyperiid amphipods in their subumbrella; and some had euphausiids and small caridean shrimps in the gut or subumbrella. Life cycle: It has been found to reproduce both sexually and asexually. At first, the egg is fertilized resulting a polyp which continues to grow asexually. Its sexual reproduction is ovoviviparous, i.e. the eggs are fertilized in the female, released by the ovary, but then continue to grow internally, which is called brooding, until they hatch. The actual larvae are released at birth. Envenomation: It is one of the five most poisonous jellyfish in the world (Anon. https://www.leisurepro.com/blog/scuba-guides/5-venomous-jellyfish-world/). It is notorious for its sting along the beaches of several localities of the Atlantic and Pacific. Though the sting itself of this species is not particularly dangerous, it can cause excruciating pain and a life-threatening reaction known as Irukandji syn drome. Unlike the true Irukandji, in which stings may barely be noticed at first, this species causes severe pain immediately following the sting. Symptoms start anywhere from within 5 to 120 min. Symptoms include headache, backache, muscle, chest and abdominal pains, nausea, vomiting, sweating, anxiety, hypertension, tachycardia and pulmonary oedema (Anon. https://en.wikipedia.org/wiki/Alatina_ alata). Unlike other cnidarians where venom is synthesized exclusively in, or nearby, nematocysts, gland cells with possible dual roles in secreting toxins and toxic-like enzymes are found in the gastric cirri of this species. Frazão and Antunes (2016) reported that this species produces toxins CaTX-A, CaTX-B and CaH-1. Remigante et al. (2018) reported that the toxin CaTX-1 produced by this species possessed haemolytic activity. 5.1 Family Alatinidae 135

Alatina moseri (Mayer, 1906) (¼ Alatina mordens)

Common name (s): Winged box jelly, outer reef Irukandji Global distribution: Tropical, Eastern Central Paciﬁc: Hawaii. Ecology: It is a pelagic species entering leeward near-shore waters. Biology Description: Bell of this species is 85 mm high and 27 mm wide; very tall and narrow; with bluntly rounded apex and without circumaboral groove; and with thin but rigid mesoglea. Exumbrella is with nematocysts but without gelatinous warts. Its broadly rounded pedalia are without pedalial nematocysts absent. Tentacles are with equal-sized nematocyst rings which are straight sided at their base. Rhopalia are with two round median eyes with lens and two lateral elongated ocelli. Gastric cirri are arranged in parallel manner and are rooted together in pairs. Gonads are found attached along bell walls and are growing outwards into the bell cavity. In preserved specimens, body is hyaline; tentacles are pink; ocelli are dark brown and gonads are milky yellow. Colour in life is unknown. Food and feeding: It feeds mainly on zooplankton. Life cycle: This species enters leeward near-shore waters to spawn about 7–10 days after the full moon. It is often attracted to bright light. During spawning gonads become cloudy and rupture in several spots along the distal axis releasing spermatozoa into the gastro-vascular cavity which were then shed through the manubrium into the water. Females take up the spermatozoa into the gastro-vascular cavity. Further, its gonads become opaque and also rupture in several spots while eggs are concurrently ovulated into gastric sacs for fertilization. Within several hours, embryos are seen circulating through the entire gastro-vascular system, the fertilized eggs are released and the planulae settle out after several days to start 136 5 Biology and Ecology of the Venomous Marine Box Jellyfish (Class Cubozoa) development as polyps. In the laboratory, polyps begin to start metamorphosis 31 days postfertilization. Envenomation: It delivers a severe sting that may be life-threatening to sensitive individuals (Anon. https://www.marinelifephotography.com/marine/cnidaria/ alatina-moseri.htm). Mercurio (2016) reported that in extreme cases of envenomation, acute heart failure appears to result from affecting neuronal sodium channels. This sodium channel effect causes a huge release of endogenous catecholamines by this jellyﬁsh. This high venom-induced release of stress-linked neurotransmitter may be responsible for cardiomyopathy (a disease of the heart muscle that makes it harder for your heart to pump blood to the rest of your body). It can lead to heart failure. Tibballs et al. (2012) reported that the syndromic illness, resulting from a characteristic relatively minor sting of this species, develops after about 30 min and consists of severe muscle pains especially of the lower back, muscle cramps, vomiting, sweating, agitation, vasoconstriction, prostration, hypertension and in cases of severe envenomation, acute heart failure. Tamanaha and Izumi (1996) reported that the sting of this species produces a mixture of toxic and allergic reactions and in acute cases results in local painful, pruritic erythematous dermatitis that may persist for 7 months.

Keesingia gigas Gershwin, 2014 Image not available Common name (s): The “giant” Keesingia Global distribution: Subtropical; Eastern Indian Ocean: Australia. Ecology: It a planktonic species. Biology Description: This species does not have tentacles. It is normally only about as big as a fingernail in size. But specimens as big as a person’s arm are also found. It can reach a maximum size of 50 cm. It has a large, thick, warty bell; with deeply incised frown-shaped rhopalial niches, divided below at the midline; with well-developed subumbrellar mesenteries and with adradial gelatinous lappets. Bell is very tall and narrow, with rigid jelly about 9 mm thick around middle portion of bell. Exumbrellar surface is fairly densely and evenly covered with thousands of small gelatinous warts over most of the body except for inside the corner furrows; and the warts do not appear to be studded with nematocysts, nor do they appear to be abraded. Corner furrows are well defined, moderately deep and are running the full length of the bell from just below the apex to the top of the pedalia. Bell is transparent and colourless, somewhat cloudy in appearance, with orange-coloured exumbrellar warts in life. Mesenteries and pedalial canals are whitish. Association: This species is associated with juvenile leatherjacket fishes, which are reported to be living inside the subumbrellar cavity. Envenomation: It is extremely venomous and is thought to cause Irukandji syndrome, a condition that can be fatal to humans. Scientists believe that the Irukandji syndrome can cause cardiac arrest within 20 min and kills its victim if not immediately treated (Anderson 2014). 5.2 Family Carukiidae 137

Manokia stiasnyi (Bigelow, 1938) ( ¼ Carybdea stiasnyi) Image not available Common name (s): Not designated Global distribution: Tropical; Western Central Paciﬁc: Indonesia. Ecology: It is a pelagic species. Biology Description: Body of this species is barrel shaped, widest in middle region and is with conspicuous apical depression. Interradial furrows are deep, nearly meeting pedalia. Adradial furrows are deep, demarcating rhopaliar region and interradial thickenings. Bell is with scattered gelatinous nematocyst warts which are extending onto velarium. Its four pedalia are interradial, scalpel-shaped, with relatively narrow inner keel and are lacking nematocyst warts or freckles. There are four branched tentacles which are interradial and are with evenly sized nematocyst bands. It has a maximum length of only 2 cm. Life cycle: In this species eggs hatch and undergo three juvenile instars before becoming adults. Envenomation: Carybdea is the only genus of venomous box jellyﬁsh in the family Carybdeidae, and has a reputation as the most venomous (Burnett et al. 1996).

5.2 Family Carukiidae

Carukia barnesii Southcott, 1967

Common name (s): Irukandji jellyﬁsh, Barnes’ jellyﬁsh Global distribution: Northern Australia from Western Australia to Queensland; off Sydney and Melbourne. Ecology: It is solitary and is usually occupying deeper offshore waters. Biology 138 5 Biology and Ecology of the Venomous Marine Box Jellyfish (Class Cubozoa)

Description: Its square-shaped bell of this species measures only 20 mm in diameter and 25 mm in height. It has four contractile tentacles, one extending from each bottom “corner” of its bell, ranging in length from 5 to 50 cm. Tentacles house the nematocysts which are stinging cells. Type I nematocysts (homotrichous microbasic rhopaloids) and Type II (homotrichous haplonemes) nematocysts are both found on the tentacles and bells of the species These cells are also capable of producing venom that changes composition as C. barnesii matures to adulthood. Protein composition of the venom of this species increases as this jellyfish alters its prey from invertebrates (zooplankton and crustaceans) to vertebrates. Food and feeding: It preys on plankton, larval fish including that of Acanthochromis sp. It feeds by stinging its prey through nematocysts and injecting venom. Once the prey is paralysed and in captivity, muscle cells in the tentacles will aid the jellyfish to bring food closer to its mouth. At the mouth, the food can enter a gastric cavity and be digested. Life cycle: Cubozoans follow a life cycle that alternates between young benthic sessile polyps and adult motile pelagic medusae. The life cycle begins with a planula larva which will continue to swim until it finds a substrate that it can use as support. Once the planula attaches to a substrate like a coral reef or rock, the organism will metamorphose into a polyp. This polyp can remain asexual for extended periods of time. Eventually, the polyp will form a polyp colony. As it continues to acquire nutrients, the colony will develop into a mature medusae adult. Envenomation: This is the first species known to cause Irukandji syndrome. It is known for producing potent venom and is known for inflicting the Irukandji syndrome which is associated with the symptoms of muscle aches, back pain, nausea, headaches, chest and abdominal pains, sweating, high blood pressure and difficulty breathing. Most reported incidents relating to this species have been localized to Australia during the warm summer season. Due to its small size, they often go undetected in the open water (Anon. https://en.wikipedia.org/wiki/Carukia_ barnesi; Tibballs et al. 2012). Bentlage et al. (2010) and Anon. (https://ucmp.berkeley.edu/cnidaria/C_barnesi. html) reported on the events associated with the stings of this species. At first, the sting is mild. About 10 min later, the skin where the sting occurred begins to sweat intensely. Within roughly 20–30 min, there are intense pains in the stomach, limbs, back and head. Breathing is difficult; vomiting or coughing may occur. It is probably lethal although this has not been definitively demonstrated. Mercurio (2016) reported that in extreme cases of envenomation of this species, acute heart failure appears to result from affecting neuronal sodium channels. This sodium channel effect causes a huge release of endogenous catecholamines by this jellyfish. This high venom-induced release of stress-linked neurotransmitter may be responsible for cardiomyopathy. Frazão and Antunes (2016) reported on the isolation of toxins CbTX-1,II from this species. 5.2 Family Carukiidae 139

Carukia shinju Gershwin, 2005 Image not available Common name (s): Irukandji jelly Global distribution: Tropical; Eastern Indian Ocean: Australia. Ecology: It is an offshore, pelagic species. Biology Description: This species has a body height of about 16 mm and is with branched velarial canals. Bell is small, rounded and bluntly pyramidal in shape. It is 16 mm tall and is with small warts scattered over bell, especially on apical region. Interradial furrows are deep along whole of bell height. Adradial furrows are also deep. Body is transparent and colourless in life. Red pigment marks nematocyst warts and tentacle bands are very pale yellow. Its four tentacles arising from each corner have aggregations of nematocysts forming distinct circular bands with an inferior margin greater in circumference than the superior margin giving an appearance described as “neckerchief-like tails”. Food and feeding: This predatory species feeds on amphipods, ﬁsh eggs, copepods, shrimps and daphnia. Envenomation: Stings of this venomous jellyﬁsh can result in Irukandji syn drome. The mechanisms of actions of its toxins are not completely understood, but evidence shows that these toxins may induce large releases of endogenous catecholamines that can lead to possible stress-induced cardiomyopathy (Anon. https://en.wikipedia.org/wiki/Carukia_shinju). Tibballs et al. (2012) reported that the syndromic illness, resulting from a minor sting of this species, develops after about 30 min and consists of severe muscle pains especially of the lower back, muscle cramps, vomiting, sweating, agitation, vasoconstriction, prostration, hypertension and in cases of severe envenomation, acute heart failure.

Gerongia rifkinae Gershwin & Alderslade, 2005 140 5 Biology and Ecology of the Venomous Marine Box Jellyfish (Class Cubozoa)

Common name (s): Not designated Global distribution: It is present in the tropical waters; Northern Territory and the Carpentian Gulf, Australia. Ecology: The species lives in near the surface. Biology Description: Bell of this species measures 60 mm long and 20 mm in diameter and is whitish-transparent. Its tentacles which are lemon-shaped measure over 1 m. Anatomy of this species is very similar to jellyﬁsh such as Morbakka, but with some signiﬁcant differences, such as the absence of horns of rhopalia or morphology of different channels of velarium. Envenomation: This species is responsible for mild form of Irukandji syndrome and the symptoms include muscle aches, vomiting, headache and nausea (Anon. http://tallanopsis.com/article/gerongia-rifkinae).

Malo bella Gershwin, 2014 Image not available Common name (s): Irukandji jellyﬁsh Global distribution: Tropical; Eastern Indian Ocean: Australia. Ecology: It is a pelagic species. Biology Description: Malo bella has a small, bell-shaped body and is 19 mm in bell height. It is with long, well-developed subumbrellar mesenteries. One tri-branched velarial canal is centrally located in each octant. Its perradial lappets are broadly rounded, with irregular rows of nematocyst warts. Rhopalial horns are short and straight. Statoliths are almost perfectly hemispherical; and tentacular nematocyst bands are with or without halo-like shelves of tissue. Colour of the bell is transparent and colourless; nematocyst warts are faintly reddish; tentacles are white and gonads are nearly opaque whitish. Envenomation: it is an extremely venomous species. Its stings are only moderately painful. However, 20–30 min later patients may develop systemic symptoms collectively known as Irukandji syndrome. The condition can cause severe abdominal pain, back, limb or joint pain, nausea and vomiting, profuse sweating and agitation. The patients may also experience numbness or paraesthesia. More severe reactions to Irukandji stings can include hypertension and tachycardia. The symptoms last from hours to weeks, and victims usually require hospitalization (Anderson 2014).

Malo filipina Bentlage & Lewis, 2012 Image not available Common name (s): Irukandji jellyfish Global distribution: Philippines. Ecology: It is a planktonic species. Biology Description: M. filipina is a small jellyfish measuring between 30 and 40 mm. Its bell which is taller than wide is white/transparent. Leaf-like gonads are seen in 5.2 Family Carukiidae 141 mature individuals. Exumbrella is with regularly spaced nematocyst warts. Stomach is reaching deep into subumbrella. Gastric phacellae are absent. Its pedalia are with thorn-like extension at pedalial canal bend. Tentacular cnidome is consisting of microbasic p-mastigophores and microbasic p-euryteles. Food and feeding: It preys mainly on rabbitfish, Siganus spp. Envenomation: Like Malo kindgi and M. maximus, stings of this species causes Irukandji syndrome. While rarely fatal, victims are often taken to hospital. It takes 5–10 min after the sting for symptoms to set in, but when they do, they are excruciating. A typical set of symptoms include severe lower back pain, vomiting and muscle cramps, and if particularly serious, these could result in toxic heart failure, fluid on the lungs or a brain haemorrhage (Reimer 2017).

Malo kingi Gershwin, 2007

Common name (s): Common kingslayer, Irukandji jellyfish Global distribution: This species is local to Queensland, Australia. Ecology: Very little is known about the ecology of this species, except that it is typically found washed up on the beach in late summer. Biology Description: Bell of this species is about 3 cm tall, half as wide, narrower at apex than base and is evenly rounded aborally. Mesoglea is fairly thick. Exumbrella is with low, round, gelatinous warts. Interradial furrows are shallow, with raised ridges along either side, running the full height of bell. Adradial furrows are poorly defined in upper half, shallowly defining rhopaliar region in lower half, but not defining interradial pillars. There are four tentacles, one per pedalium. In life, the bell is transparent and colourless; tentacles are faintly pink and exumbrellar nematocyst warts are pale purple. Envenomation: It has some of the world’s most potent venom. As an Irukandji, it can cause Irukandji syndrome, characterized by severe pain, vomiting and rapid rise in blood pressure. The death of Robert King is the only proof of its deadly venom. There have also been other incidents of its stinging people and associated fatality off North Queensland, Australia (Bentlage et al. 2010; Gershwin 2007; Wikipedia). Frazão and Antunes (2016) reported on the presence of toxins MkTX-A,B from this species. 142 5 Biology and Ecology of the Venomous Marine Box Jellyfish (Class Cubozoa)

Malo maxima Gershwin, 2005

Common name (s): Irukandji jellyfish Global distribution: Tropical; Eastern Indian Ocean: Australia. Ecology: Specimens of this pelagic species have been caught nearshore during onshore winds but observed to be more common offshore. It often occurs in a band, about 9 m deep. Most often caught during the penultimate hour before slack tide, with higher abundance on a falling tide than on a rising tide. Biology Description: It is a small and extremely venomous Irukandji jellyfish. It has a transparent, cubic to pyramidal bell which is covered with colourless nematocyst warts and a long, scalpel-shaped pedalia with straight pedalial canals which are having rectangular knee bends with a short projection and single pinkish tentacles. Rhopalial niche orifices are frown-shaped and located at about 1/6 to 1/5 up the bell rim. All animals have a velarium with four, triangular perradial lappet pairs and four to five single-rooted velarial canals per octant. Stomach is with a very short manubrium which is bag-shaped and connected by well-developed mesenteries to the subumbrella. Gonads of the immature animal are arrow-head shaped, with the widest part above the rhopalial niche. In mature animals, the gonads are large and leaf-like; and they overlapped perradially, leaving a space around the rhopalial niches. Envenomation: Its stings are potentially fatal as it causes a severe form of Irukandji-like syndrome (Wikipedia). Mercurio (2016) reported that in extreme cases of envenomation of this species, acute heart failure appeared to result from affecting neuronal sodium channels. This sodium channel effect caused a huge release of endogenous catecholamines by this jellyfish. This high venom-induced release of stress-linked neurotransmitter may be responsible for cardiomyopathy. The syndromic illness, resulting from a characteristic relatively minor sting of this species, develops after about 30 min and consists of severe muscle pains especially of the lower back, muscle cramps, vomiting, sweating, agitation, vasoconstriction, 5.2 Family Carukiidae 143 prostration, hypertension and in cases of severe envenomation, acute heart failure (Tibballs et al. 2012).

Morbakka fenneri Gershwin, 2008

Common name (s): Fire jellyfish Global distribution: Warm waters of eastern and northern Australia. Ecology: It lives in the calm waterways and marinas. Biology Description: It has a solid body with bright pink, wart-like protrusions on the top. Its transparent, box-shaped bell is up to 5 cm wide and 10 cm tall. Bell has evenly thick mesoglea of rigid consistency and is with straight sides and flat to shallowly rounded top. Exumbrellar surface is with numerous gelatinous warts, especially concentrated apically; and coronal furrow is absent. Interradial furrows are deep and well marked, extending to just above point of subumbrellar lamellae. Adradial furrows are deep in lower half, with well-defined interradial pillars and per radial “smile lines”; and upper half is shallower. There are four flat, ribbon-like tentacles which grow as long as 1 m. No information presently exists as to its general behaviour, life cycle or predator– prey relationships. Envenomation: Anon. (https://www.lakesmail.com.au/story/5443913/researcher- details-extent-of-lake-jellyfish-danger/) and Tibballs et al. (2012) reported that though there have been no reported fatalities, the sting of this jellyfish has the potential to make one very sick. Stings from this species can range from skin pain to mild or severe in Irukandji syndrome. The symptoms of the syndrome include severe headache, backache, muscle pains, chest and abdominal pain, nausea and vomiting, sweating, anxiety, hypertension and tachycardia. 144 5 Biology and Ecology of the Venomous Marine Box Jellyfish (Class Cubozoa)

Gershwin (2008) reported that this jellyﬁsh is capable of inﬂicting a severe sting which may include symptoms similar to Irukandji syndrome, a life-threatening case, in which heart damage occurred, though this is exceptional.

Morbakka virulenta (Kishinouyea 1910) ( ¼ Tamoya virulenta) Image not available Common name (s): Japanese giant box jellyfish Global distribution: Tropical and temperate waters; Seto Inland Sea; off the coast of Japan. Ecology: This planktonic species lives in the neritic zone. Biology Description: It has a box-like shaped body with rabbit-ear-like rhopaliar horns. It is one of the largest species of box jellyfish, with tentacle lengths of about 3 m at maximum extension. Its maximum bell height is 250 mm and bell width is 200 mm. Bell of this species is rectangle-shaped and is covered with nematocyst warts. This species can be distinguished from other species in the family by its heavily branched velarial canals as well as two rows of perradial warts with additional scattered warts. Food and feeding: It is a piscivorous species feeding mainly on the Japanese anchovy. Its nocturnal occurrence near the surface often takes place around the slack tide, during which the medusae forage with tentacles fully extended. Predators: Black scraper, Thamnaconus modestus, a species of filefish. Association: Commensalism has been reported in this species with juvenile Japanese horse mackerel. Life cycle: This species prefers to breed in the morning time during the fall and winter months, the only months in which adult specimens have been observed. The metamorphosis of embryo into primary polyps has been observed to take a period of 21 days, significantly longer than other box jellyfish. Due to the soft bottoms over which this jellyfish breeds, the polyps have long stalks to compensate for being buried in the soft sediment layer on the seafloor. The metamorphosis from polyp to juvenile medusa takes 15 days under the right conditions, and the full maturation of the medusa takes approximately 100 days. Envenomation: This jellyfish has led to many envenomation problems in Australia (Anon. http://www.marine-medic.com.au/pages/thesis/thesisBreakup/5_ 7.pdf). While this species is known by local fishermen and divers as a dangerous species and has been described as having a fiery sting, it has not yet been confirmed if it contains the toxic venom that causes Irukandji syndrome, which can lead to heart failure and death (Anon. https://en.wikipedia.org/wiki/Morbakka_virulenta). 5.3 Family Carybdeidae 145

5.3 Family Carybdeidae

Carybdea arborifera Maas, 1897

Common name (s): Not designated Global distribution: Tropical; Eastern Central Paciﬁc: Hawaii. Ecology: It is a member of zooplankton. Biology Description: Bell of this species is blunt pyramidal; highly transparent and is regularly scattered with small, colourless, nematocyst warts, from apex to bell margin. Bell height reaches 30 mm and bell width 33 mm. Mesoglea is thin. Gastric phacellae are epaulette shaped, single rooted and are multiple stemmed. There are two velarial canals per octant. Food and feeding: It feeds on crab zoeae, shrimp larvae, copepods and ﬁsh larvae. Envenomation: Tibballs et al. (2011) reported that the sting of this species may cause allergic dermatitis. 146 5 Biology and Ecology of the Venomous Marine Box Jellyfish (Class Cubozoa)

Carybdea branchi Gershwin & Gibbons, 2009

Image credit: Wikimedia commons Common name (s): South African box jellyfish Global distribution: Subtropical; south-east Atlantic: South African coast to Port Elizabeth. Ecology: This pelagic species lives from the surface to a depth of at least 35 m. It is often seen in swarms. Biology Description: Robust and well-sculpted body; gastric phacellae epaulette-shaped, single-rooted, multiple-stemmed; velarial canals three per octant; complexly branched; pedalia knee bend upwards turned volcano-shaped. The brownish pigmentation of the phacellae and pedalia is characteristic of this species. This small box jellyfish has a transparent box-shaped bell with a very long tentacle (up to 2 m) trailing from each corner. Bell is 68 mm in height and 80 mm in width. It is with thick, rigid mesoglea especially apically. There are numerous oblong to amorphous small unraised or slightly raised nematocyst warts scattered densely over entire exumbrella. Coronal indentation is shallow just below apex. Interradius is thickened throughout bell height with deep median furrow reaching all the way to pedalium. Adradial furrows are strongly pronounced deeper in lower half of the bell. Perradius is smooth, raised with rhopaliar niches surrounded by deep horseshoe-shaped furrow. Colour of the bell is slightly translucent with pigmentation. A single small red blotch is present on the apical portion of exumbrella above each of the four phacellae, and single faint brownish blotch is seen at shoulder of each of the four pedalia. Tentacles are whitish to faintly pinkish. Predators: It is eaten by the sunfishes, Mola mola and Mola ramsayi, as well as the slender sunfish, Ranzania laevis. 5.3 Family Carybdeidae 147

Envenomation: The tentacles of this venomous species have a painful sting although the sting is not known to be fatal (Anon. https://en.wikipedia.org/wiki/ Carybdea_branchi, https://www10.dict.cc/wp_examples.php?lp_id¼1&lang¼en& s¼box%20jellyﬁsh). Gershwin and Gibbons (2009) reported that the sting of this species lead to acute ﬁre-like pain which is lasting about 10 min; and cessation of heart beat which is followed by abnormally rapid heart beats.

Carybdea brevipedalia Kishinouye, 1891

Common name (s): Not designated Global distribution: Pacific Ocean: Korea (South Sea), Japan. Ecology: It is a member of zooplankton found in coastal waters. Biology Description: Bell of this species is highly transparent, colourless, bell-shaped and is regularly scattered with very small, colourless, equal-sized nematocyst warts, from apex to bell margin. Apex is convex; mesoglea is thick and there is a slight horizontal constriction near the top. Bell is up to 35 mm high, and width is up to 33.5 mm. There are four gastric phacellae which are linear-shaped and are located in the corner of stomach. Each phacella comprises multiple roots of cirrus bundles, and each root 148 5 Biology and Ecology of the Venomous Marine Box Jellyfish (Class Cubozoa) has multiple numbers of cirri. Gonads are leaf-shaped, attached on four corners of inner wall in subumbrellar cavity and are covering almost full length of lateral inner bell. Manubrium is four branched and its length is approximately one-third (sometimes elongates to one half) of height of subumbrellar cavity. Inner wing of pedalia is scalpel-shaped. Nematocyst warts are scattered on outer pedalia with a row of larger ones near the outmost edge; and there are no nematocyst warts on inner wing of pedalia. Four rhopalia are present in rhopalia niche, which is located one-fourth downward part of bell. One tentacle is present on each corner of bell. Velarial canals are transparent in live samples, while dark-coloured in fixed ones. Food and feeding: It feeds on Artemia and other jellyfish. Life cycle: In this species, fertilization occurs externally. Fertilized eggs develop into blastulae within 6 h. These blastulae develop into planulae bearing about 30 larval ocelli within 12 h, and then settle in 2–3 days and metamorphose into primary polyps bearing one to four tentacles. Primary polyps develop into adult polyps within 80 days. Budding occurs in three to four tentacled polyps, and buds are released 2 days after the commencement of budding. Envenomation: Kitatani et al. (2015) reported that this harmful, stinging jellyfish species caused moderate to severe pain. Its nematocyst tubules are longer than 200 μm and are sufficiently long to penetrate the human epidermis and physically stimulate the free nerve endings of Aδ pain receptor fibres around plexuses to cause acute pain and inject the venom into the human skin epithelium to cause persistent pain and inflammation. Bentlage et al. (2010) reported that this species had the highest haemolytic activity. 5.3 Family Carybdeidae 149

Carybdea marsupialis (Linnaeus, 1758)

Image credit: Wikimedia Commons Common name (s): Warty sea wasp Global distribution: Subtropical; Eastern Central Pacific, Western Central Atlan- tic and the Mediterranean; north Italian Adriatic coast. Ecology: It is a benthopelagic species present in the upper few metres of the sea; also inhabits near shore, mangrove channels and kelp forests; depth range is 0–20 m. Biology Description: It is a small transparent jellyfish with a box-shaped bell which is sturdy and is slightly wider than its height. Bell height is up to 40.5 mm and bell width is up to 40 mm. At the four lower corners of the bell, there are four elongated tentacles which are up to 30 cm long. Bell has a number of small white or yellowish warts with stinging cells, and near the margin, equidistant from the tentacles, are four rhopalia (sensory structures with ocelli). This species can be distinguished from other similar species by the red banding on the tentacles. Interradial furrows are shallow and are highly transparent with few whitish nematocyst warts sparsely scattered on bell from apex (very small warts) to bell margin (big warts along 150 5 Biology and Ecology of the Venomous Marine Box Jellyfish (Class Cubozoa) interradial furrows). Apex is thickened and domed, with slight horizontal constriction at level of gastric phacellae. Food and feeding: It preys on plankton such as copepods, mysids and gammarids. As a predator, it also feeds on invertebrates and even small fish which it captures with the nematocysts (stinging cells) in its tentacles, often in shallow waters. Life cycle: The life history of this box jellyfish is complex. The sexes are separate and sexual reproduction takes place with the emission of gametes into the open water. After fertilization, a planula larva forms which later develops into a cubopolyp with a few tentacles. This can reproduce asexually by budding and the buds become detached. At first they creep across the substrate with the tentacular region leading. During this mobile stage, pieces may become detached or the cubopolyp may split transversely; and these fragments regenerate their missing parts within 72 h. The resulting polyps then attach themselves to the substrate and grow a full complement of 24 tentacles. About a month later they become detached, the multiple tentacles are reabsorbed and the four tentacles typical of the medusa phase develop. Envenomation: The sting of this species is venomous to humans. In severe cases, the symptoms can be systemic, including pain, paraesthesia, hyperesthesia and skin lesions (Anon. https://en.wikipedia.org/wiki/Carybdea_marsupialis). Anon. (http://www.cmas.org/news/watch-out-for-the-gelatinous-organisms-of- the-eastern-mediterranean) reported that this box jellyfish can inflict a painful, albeit non-lethal sting. A woman stung by this species at a Spanish Mediterranean beach showed systemic manifestations over several months [pain far from the inoculation point, arthralgia, paraesthesia, hyperesthesia, increase in eosinophils and immunoglobulin E (IgE)] in addition to the skin condition (Bordehore et al. 2015). Montgomery et al. (2016) reported that the sting severity of this species is high. Mariottini (2014) reported on the presence of a cytolysin of nematocyst venom viz. cartox from this species. This pore-forming protein was found to be haemolytic on human and sheep RBCs. 5.3 Family Carybdeidae 151

Carybdea rastoni Haacke, 1887

Common name (s): Box Jellyfish (sea wasp), jimble Global distribution: Very rare in Southern California; more commonly seen in tropical waters around Hawaii, Australia, Japan and the Philippines. Ecology: It lives in shallow coastal waters. Biology Description: Bell of this species is cube-like shape with four flattened sides. Its height is 30–35 mm and bell width is 20–30 mm; and it is highly transparent, colourless, slightly higher than wide and is regularly scattered with colourless, nematocyst warts, from apex to bell margin. These warts are more dense on the bell sides than on the bell edges. Nematocysts are roundish to oval with different diameters, and the largest is approx. 0.5 mm in diameter. Velarium is without nematocyst warts. Mesoglea is thick. One long tentacle comes from each corner of this cube. Pinkish-brown gonads are visible when viewed from above. Food and feeding: It preys on mysids, larval fish; crab zoeae, shrimp larvae and copepods. 152 5 Biology and Ecology of the Venomous Marine Box Jellyfish (Class Cubozoa)

Envenomation: This jellyfish which has a painful sting is one of the most bothersome stinging pests to swimmers and bathers on the Japanese coast. From tentacles of this jellyfish, five highly haemolytic proteins (CrTX-I, CrTX-II and CrTX-III; CrTX-A and CrTX-B) have been purified (Mariottini 2014; Remigante et al. 2018). Frazão and Antunes (2016) reported on the occurrence of toxins CuTX-A and CyTX-B from this species.

Carybdea xaymacana Conant, 1897 Image not available Common name (s): Jimble Global distribution: Tropical; Western Central Atlantic: Jamaica, Haiti, Bermuda and Caribbean. Ecology: This pelagic species is found on the surface of calm, shallow waters. Biology Description: Bell of this species is highly transparent, colourless, bell-shaped and is scattered with very small colourless nematocyst warts (bigger nematocyst warts are at interradial furrows and smaller nematocyst warts on bell sides). Apex plane is convex. Bell height is up to 24 mm and width is up to 27 mm. Food and feeding: It prey on polychaetes (Ceratonereis sp.), crustaceans (Acartia sp.), ﬁsh (Jenkinsia sp.), and eel larvae. Envenomation: Venom from this species may cause pore formation in myocardial cellular membrane (Mercurio 2016). Mariottini (2014) reported that the whole nematocyst venom of this species showed hemolytic activity against sheep and human erythrocytes, causing 100% hemolysis within minutes. Tibballs et al. (2012) reported that syndromic illness, resulting from a characteristic relatively minor sting, develops after about 30 min and consists of severe muscle pains especially of the lower back, muscle cramps, vomiting, sweating, agitation, vasoconstriction, prostration, hypertension and in cases of severe envenomation, acute heart failure resulted. 5.4 Family Chirodropidae 153

5.4 Family Chirodropidae

Chirodropus gorilla Haeckel, 1880

Image credit: Wikimedia Commons Common name (s): Box jellyfish Global distribution: Subtropical; Eastern Central Atlantic: Liberia, South Africa and Western Africa. Ecology: It is a member of zooplankton. Biology Description: It is a large, cuboid medusa. Its bell height is up to about 15 cm and width is 12 cm, nearly flat-topped and is probably without prominent vertical flutings on sides and corners. Bell is translucent blue-white with a few vertical brown stripes. Jelly is thick and rigid. Velarium is wide (1/6 bell height) and thin velarial canals are 20+ per quadrant, tortuous, some are with large forkings and all with short side branches. Rhopalia is 1/4 way up from bell margin. Its four pedalia are found inserted along 1/3 of bell height. There are up to 12 tentacles which are found on each bell corner. Gastric pouches (4) are bearing conspicuous finger-shaped processes hanging down into the sub-umbra space. Gonads (4) are seen under the top of the subumbrellar cavity, like bunches of grapes in shape. Food and feeding: It feeds on small shrimp or fish. Association: The subumbrella of this species has cardinalfish, Nectamia sp. Envenomation: It is one of the most venomous box jellyfish (Blaxter et al. 1984; Anon. http://www.namibiandolphinproject.org/animals/hall-of-fame/chirodropus- gorilla/). 154 5 Biology and Ecology of the Venomous Marine Box Jellyfish (Class Cubozoa)

Chironex ﬂeckeri Southcott, 1956

Common name (s): Box jellyfish, sea wasp or marine stinger Global distribution: Tropical Indo-West-Pacific Ocean; from northern Australia and New Guinea north to the Philippines and Vietnam Found in coastal waters off North Australia throughout Indo-Pacific. Ecology: It tends to inhabit shallow, murky saline waters at depths of 39–56 m. These animals also inhabit shallow rivers during the reproductive season and during their polyp stage. Once young jellyfish mature into medusa, they follow the river out to sea. Biology Description: This jellyfish is the largest of the cubozoans weighing 2–6 kg. It is square in shape, and it can grow to be as big as a baseball. There is a large umbrella- like bell with four bundles of tentacles arising from the corners of the bell. From each of the four corners of the bell trails a cluster of 15 tentacles which are up to 5 m long. Each tentacle contains millions of nematocysts, which are microscopic hooks where venom is held and delivered. It has four eye clusters with 24 eyes. Their 60 tentacles are each 4.5 m long. This species is pale blue in colour and is with radial symmetry. 5.4 Family Chirodropidae 155

With only a single opening (the mouth and entrance to the cavity), its body encompasses a single sac-like body space. Food and feeding: It feeds mainly on small fish and shrimps. It tends to feed primarily on the shrimp, Acetes australis. This jellyfish relies on their venomous tentacles to capture its prey. The millions of nematocysts on its tentacles deliver lethal doses of venom to its prey, immobilizing or killing them in a short amount of time. It is a day hunter as it is seen resting on the ocean floor at night. Predators: The only known predator of this box jellyfish is the green turtle Chelonia mydas, which is unaffected by its stings as the venom of this jellyfish does not penetrate turtle’s thick skin. Life cycle: In the sexual reproduction, this jellyfish develops planulae which soon develop into polyps. These polyps are sessile and small (1–2 mm) with two tentacles. Polyps use these tentacles to attach to a hard surface. A polyp can reproduce asexually via budding. After a polyp has metamorphosed into a small medusa, it travels from freshwater rivers to the sea. Once in the sea, a maturing box jellyfish continues to grow until it reaches its full size. The life span of this species is about 1 year only as it dies shortly after spawning. Envenomation: This species has been identified as “the most lethal jellyfish in the world”, causing Irukandji syndrome. A total of 63 deaths have been reported in Australia from 1884 to 1996. It is posing a danger to swimmers since its transparency makes it difficult to see in the water. Envenomation (or stinging) of this jellyfish occurs when human skin contacts the thousands of densely packed nematocysts that line the jellyfish tentacles. Immediately after contact, the nematocyst capsules fire thousands of barbed, poison-filled darts. Each poison-filled dart is filled with porins (transmembrane proteins), neurotoxic peptides and bioactive lipids. The amount of venom in one animal is said to be enough to kill 60 adult humans, although most stings are mild and do not require hospitalization (Due 2017). Local signs (skin symptoms) of this box jellyfish occur immediately upon contact and include exquisite pain, itch and welts at the area of contact; linear welts are a brownish-purple colour and up to 10 mm in width; lesions may be visibly haemorrhagic; blisters may form within minutes of contact; full-thickness skin necrosis can occur 1–2 weeks later; and it can be followed by whip-like hypopigmentation or hyperpigmentation. Systemic signs of this box jellyfish envenomation include difficulty breathing, drop in blood pressure, irritability and restlessness, faintness and collapse, cardiac arrhythmias and cardiac arrest. The response to this box jellyfish envenomation however varies from person to person, depending on how well the dermis can clear irritant chitins (the jellyfish exoskeleton) from the skin (Due 2017). Cadogan (2019) reported that this box jellyfish possesses extremely powerful and (possibly) fatal sting. Severe envenoming of this species has been associated with at least 67 deaths in Australia. All deaths occurred within 5 min of the sting, probably secondary to direct cardiac toxicity. Brinkman et al. (2014) reported that the venom of this species is the deadliest venom on earth. It has been known to cause deaths in the tropical waters of Australia and the Indian Ocean, with about 70 deaths recorded in the twentieth century. 156 5 Biology and Ecology of the Venomous Marine Box Jellyfish (Class Cubozoa)

Anon. (https://www.leisurepro.com/blog/scuba-guides/5-venomous-jellyfish- world/) reported that the venom of this most dangerous jellyfish species is the strongest of any species of jellyfish as it has the ability to kill an adult man with a dose that weighs about as much as a single grain of salt. One sting can result in extreme pain and excruciating burning sensations; if left untreated, it can cause cardiac arrest and death. Mariottini (2014) reported that the venom of this species possesses hemolytic activity and cardiotoxic to Guinea pigs’ atria. Frazão and Antunes (2016) reported on the presence of toxins CfTX-1, CfTX-2, CfTX-A and CfTX-B from this species. Mustafa et al. (1995) reported that the toxin of this species was found to show cardiotoxic effects with increase in Na+ influx into the cell and further increase of intracellular [Ca2+] via the Na+/Ca2+ exchange mechanism, thus producing the observed Ca2+ overload.

Chironex indrasaksajiae Sucharitakul, 2017

Image credit: Phuping Sucharitakul, Siriwadee Chomdej, Thunyaporn Achalawitkun and Isara Arsiranant Common name (s): Not designated as it is a new species Global distribution: Thailand. Ecology: It was collected from the gulf waters. Biology Description: Live specimens of this species are cube-shaped with transparent bell. Its maximum bell height is 170 mm and maximum bell width is 136 mm. Manu- brium length is about 2/3 of bell height. There are 4 pedalia which are claw-like with up to 12 tentacles. Pedalial canal knee bend is bulbous-shaped. Tentacles are ﬂat in life and are rounded in preserved specimens. Envenomation: This species has been reported to be responsible for envenomation and documented in the Gulf of Thailand. However, detailed work on the speciﬁc toxicity and biology of this species is needed (Sucharitakul et al. 2017). 5.4 Family Chirodropidae 157

Chironex yamaguchii Lewis & Bentlage, 2009

Common name (s): Box jellyfish Global distribution: Around Japan, on Okinawa and the Ryukyu Islands, and in Philippines. Ecology: It is found in coastal waters. Biology Description: Medusa of this species is box-shaped, and it has a maximum height of about 110 mm. Its maximum interradial diameter is 95 mm. Outer surface of the bell is smooth in adults; however, bells of juvenile jellyfish are warty. There are four short stalks known as pedalia which carry up to nine tentacles. Its nematocyst threads are lavender. Manubrium is cross-shaped with lancet-shaped lips. It measures only about three quarters of the bell height. There are four rhopalia and each of them has six eyes, two with lenses and two each of slot and pit pigment eyes. Statolith is oval and is located at the base of each rhopalium. There are eight different types of stinging cells. Food and feeding: It feeds on mysids and larval fish. Envenomation: This species is highly venomous. The stings cause great pain and have caused several deaths in Japanese waters. The symptoms include cardiac arrest and respiratory failure with acute pulmonary oedema (Anon. https://en.wikipedia. org/wiki/Chironex_yamaguchii). Bentlage et al. (2010) and Anon. (https://www.sciencedaily.com/releases/2009/ 11/091118151141.htm) reported that this species has caused human fatalities in Japan and the Philippines. 158 5 Biology and Ecology of the Venomous Marine Box Jellyfish (Class Cubozoa)

Horiike et al. (2015) reported that this jellyfish yielded allergens which caused sting dermatitis. Further these stings also caused painful, papular-urticarial eruptions due to the immediate allergic, acute toxic and persistent inflammatory responses. Kitatani et al. (2015) reported that this species which is causing moderate to severe pain has nematocyst tubules longer than 200 μm, compared with a jellyfish species that cause little or no pain, Aurelia aurita. The majority of the tubules of harmful jellyfishes, C. yamaguchii and C. brevipedalia, were sufficiently long to penetrate the human epidermis and physically stimulate the free nerve endings of Aδ pain receptor fibres around plexuses to cause acute pain and inject the venom into the human skin epithelium to cause persistent pain and inflammation.

5.5 Family Chiropsalmidae

Chiropsalmus quadrumanus (Muller, 1859)

Common name (s): Four-handed box jellyfish, sea wasp Global distribution: Subtropical; western Atlantic Ocean, the Gulf of Mexico and the Pacific Ocean. Ecology: This pelagic species is found both in neritic and in estuarine environments; gulf and bay and open waters; and depth range is 0–85 m. The jellyfish were seldom seen near the surface, but small specimens were frequently taken in shrimp trawls. After gales large quantities of this species have been found washed up on the beach, and after heavy rains, many dead jellyfish were found 5.5 Family Chiropsalmidae 159

floating on the surface. When conditions returned to normal, the jellyfish disappeared. Biology Description: Bell of this species is cube-shaped, colourless and transparent with a diameter of about 14 cm and height of 10 cm. Body is composed of a gelatinous material and the top edges are rounded while the top surface is flat. There are four muscular, hand-shaped fleshy pads (pedalia) hang from bottom of the bell and each with seven to nine fingers. Each finger gives rise to a long (3–4 m) stinging tentacle. Wart-like stinging bumps are seen on the wall. Halfway up the inside of the bell is the velarium, a horizontal ring of tissue partially blocking the aperture. Manubrium is a central column hanging down inside the bell with the mouth at its tip. Its rounded stomach has four pouches connecting to radial sinuses along the edges of the bell. Gonads are seen on either side of the radial canals. Food and feeding: It preys on crustaceans: sergestid shrimp (Peisos petrunkevitchi), peneoidean and caridean shrimps, Lucifer, brachyura larvae, isopods and crabs; and nematodes, fish and fish eggs. Envenomation: The sting of this species is venomous and dangerous to humans, especially children. Its long tentacles which are armed with nematocysts can inflict an extremely painful sting on people that encounter them. All these stings have been reported to be linear in nature, causing both intense pain and systemic symptoms. Apart from pain, the symptoms included cardiac dysfunction and respiratory depression. The rash lasted for several months (Bengtson et al. 1991; Anon. https://en. wikipedia.org/wiki/Chiropsalmus_quadrumanus). Anon. (http://txmarspecies.tamug.edu/invertdetails.cfm? scinameID¼Chiropsalmus%20quadrumanus) reported that this species is extremely venomous, and it has been known to kill people within minutes of being stung.

Chiropsalmus sp. Envenomation: Mariottini (2014) reported that the whole nematocyst venom of this species has shown hemolytic activity against sheep and human erythrocytes, causing 100% hemolysis within minutes. 160 5 Biology and Ecology of the Venomous Marine Box Jellyfish (Class Cubozoa)

Chiropsoides buitendijkii (Horst, 1907)

Common name (s): None Global distribution: Indo-Pacific: India, Thailand (Andaman Sea), Malay Archi- pelago and Indochina. Ecology: It lives in mangrove forests and other coastal ecosystems. As passive swimmers, they will move closer to shore during the neap tide when sea currents are weak. Biology Description: This species has a cuboidal bell which is with a rounded dome- shaped apex. Its smooth exumbrellar surface is without nematocyst warts. Thick mesoglea is seen at bell apical and interradial pillars. Adradial body walls have thinner mesoglea layer which is becoming thicker in upper half of the bell. Adradial furrows are shallow in lower-half bell and they disappear in upper bell. Interradial furrows are absent. Envenomation: This is the most dangerous species especially for swimmers (Anon. https://www.thestar.com.my/news/nation/2017/10/08/boxy-terror-set-to- sting-penang-scientists-call-for-caution-as-deadly-box-jellyfish-found-off-states/ #FqHLKV3UjgzBC5YZ.99). Chiropsoides buitendijki has been identified as causative agent in severe envenomation in Thailand (Chaiyakul 2017). 5.5 Family Chiropsalmidae 161

Chiropsoides quadrigatus (Haeckel, 1880) ( ¼ Chiropsalmus quadrigatus)

Common name (s): Box jellyfish Global distribution: Indo-Pacific and Western Atlantic Ocean. Ecology: It is a deep-sea species. Biology Description: Bell of this transparent animal is dome-shaped and is 130 mm in width and 90 mm in height. There are four large, hand-shaped pedalia. Each of these pedalia gives rise to seven finger-like branches which are long, slender, ribbon-like tentacles. All these finger-like branches are in one direction. Stomach is wide and globular. and mouth is surrounded by four large, triangular lips. There are four interradial, crooked, crescent-shaped rows of gastric cirri on inner walls of stomach. The specimen is transparent. Food and feeding: It is believed that the unusual tentacles of this species are more suited to catching fish rather than the crustaceans and other jellies that normally fall prey to its related species. Envenomation: Bentlage et al. (2010) reported that this species has caused human fatalities in Japan and the Philippines. Mariottini (2014) reported that this species is responsible of three fatal cases in Japan. The remarkable danger of this species is largely due to the length and size of its tentacles, which allow the injection of large doses of toxin. Anon. (http://www.vapaguide.info/catalogue/NORAM-CNI-144) reported that it occurs all year round. And due to its shallow water habitat, it represents a severe danger for bathers, especially as it is practically transparent and thus very hard to see. Anon. (https://www.leisurepro.com/blog/scuba-guides/5-venomous-jellyfish- world/) reported that the very painful sting of this species can cause cardiac arrest, respiratory failure with acute pulmonary oedema, or death. Mariottini (2014) reported that this species showed haemolytic activity. 162 5 Biology and Ecology of the Venomous Marine Box Jellyfish (Class Cubozoa)

Frazão and Antunes (2016) reported on the isolation of the toxin CqTX-A from this species.

5.6 Family Chiropsellidae

Chiropsella bart Gershwin & Alderslade, 2007 Image not available Common name (s): Not designated Global distribution: Northern Territory, Australia. Ecology: It can congregate in groups of hundreds or thousands of specimens on beaches or in shallow, coastal waters. Biology Description: Bell of this species is strongly cuboid and is reaching a maximum height of 5 cm. Body mesoglea is thick and relatively solid, with thickened and stiff apical dome and interradial pillars. Its sub-apical coronal furrow is shallow and interradial, and adradial furrows are well-defined. Adradial furrows extend laterally at level of stomach, forming a well-defined rectangular perradial region. Exumbrellar surface is smooth, lacking nematocyst warts or freckles. Pedalia are long, scalpel- shaped and are with pronounced adaxial keel. Abaxial tentacle starts distally well past halfway point; and remaining fingers and tentacles are arranged close together more or less terminally, but opposite rather than alternate. Pedalial canal is flattened in cross section, with a volcano-shaped upward-pointing diverticulum near base. Sub-terminally, pedalial canal is bifurcated. Pedalial canals are straight at tentacle insertion. Tentacles are up to five per pedalium. Envenomation: This species is not known to be harmful to humans, aside from a localized painful sting. The sting of this species produces only mild pain and itching, usually persisting less than 2 h (Gershwin and Alderslade 2006).

Chiropsella bronzie Gershwin, 2006 Image not available Common name (s): Box jellyﬁsh Global distribution: Its distribution is restricted to tropical Queensland ranging from Cooktown to Townsville. Ecology: It lives in shallow water off the sandy beaches. Biology Description: In this species, the pedalial canal bend is knee-like. There are nine tentacles which are ﬁne and round. Pedalial keels are absent; Gastric saccules are separate. Envenomation: Winter et al. (2007) reported that the venom of this species is less cardiotoxic and produced a sustained contraction of endothelium-denuded aorta.

Chiropsella rudloei Bentlage, 2013 Image not available Common name (s): Not designated as it is a new species 5.7 Family Tamoyidae 163

Global distribution: North-west Madagascar. Ecology: It dwells in coastal wetlands including mangroves. Biology Description: In this species, exumbrella is smooth and is lacking nematocyst warts. Its bell height is 25–40 mm and width is 20–32 mm. Interradial gonads are well developed and are appearing mature and ripe with eggs or sperm, even in small specimens. There are 5–11 round tentacles which are truncated to short stumps. These gonads also have lateral, wing-like extensions. Food and feeding: It feeds on small shrimp or ﬁsh. Envenomation: The potency of the venom of this species remains unknown, but stings at the time of collection were mild. Care should therefore be taken when handling specimens, even though Chiropsella species are not known to inﬂict stings as severe as other chirodropids (Bentlage 2013).

5.7 Family Tamoyidae

Tamoya bursaria Haeckel, 1880 Image not available Common name (s): None Global distribution: Paciﬁc. Ecology: It lives in near-shore habitats above the continental shelves. Biology Description: Umbrella of this species is box-shaped, reaching 7 cm in diameter and 22 cm in height. Both young and adult forms of this species have the same sculptured exumbrella, i.e. with a smooth body surface. There are four wide strong corner pillars in the umbrella. Rim of the umbrella is thickened but does not show as many thickenings and prismatic laces. Its four furrows that cut the cornerstones in half approach the apex and stand there by four slightly curved transverse grooves. Envenomation: Anon. (https://kotobank.jp/word/火水母-1752401) reported that this species is highly toxic and causes severe inﬂammation when touched. This species has led to many envenomation problems in Australia (Anon. http:// www.marine-medic.com.au/pages/thesis/thesisBreakup/5_7.pdf).

Tamoya gargantua Haeckel, 1880 Image not available Common name (s): Warty sea wasp Global distribution: Tropical; Eastern Central Pacific and Indian Ocean: Eastern Africa, Samoa, East coast of India, Mergui Archipelago, Arabian sea, North Amer- ica; Malay Archipelago; New Southwales, Australia; Iranian Gulf; Japan; Samoa Islands; New Guinea. Ecology: This pelagic species lives in shores and bays. Biology Description: Bell of this species is 65 mm in height and 45 mm in diameter. Length of tentacle is 185–198 mm. Pedalia are with a sharp outer and inner edge and 164 5 Biology and Ecology of the Venomous Marine Box Jellyfish (Class Cubozoa) are pyramidal at the base and flattened near apex. Velarial canals end in trident-like distal branches. Envenomation: This is a venomous jellyfish (Anon. https://en.wikipedia.org/ wiki/Tamoya_gargantua) and its venomology is to be known.

Tamoya haplonema Muller, 1859

Common name (s): Sea wasp Global distribution: Tropical; Western Atlantic; Uruguayan waters. Ecology: This benthopelagic species lives in coastal waters; depth range is 0–85 m. Biology Description: Bell of this species is elongate-cuboid, glassy-transparent and is somewhat rigid with flat top. It is 220 mm long and its length:breadth ratio is increasing with size. Exumbrella, pedalia and velarium are covered with nematocyst warts. Velarium is much-branched. There are four pedalia and their length is approx. 2/5 of bell height. These pedalia are scalpel-shaped and sharp-edged. There are four rhopalia which are complex in structure. Its four tentacles of 3 m length when 5.7 Family Tamoyidae 165 contracted are approx. as long as bell height and are with regularly spaced nematocyst bands. Stomach is occupying up to 1/3 of length of the bell; and gastric cirri are in four vertical interradial groups (in radii of bell corners). Bell is glassy-transparent; exumbrellar warts are translucent; tentacles are milky yellow and rhopalial photoreceptors are brown. Food and feeding: It preys mainly on fish during night hours. Association: This cubozoan medusa has an association with stromateid fish, Peprilus cf. crenulatus (Lawley and Faria 2018). Envenomation: This species is known to inflict serious stings which are painful. These stings caused injuries but were not lethal (Haddad et al. 2002; Stalkers https:// jellyfish.appstate.edu/tamoya-haplonema). Anon. (http://www.marine-medic.com.au/pages/thesis/thesisBreakup/5_7.pdf) reported on the envenomation problems of this species in Australia.

Tamoya ohboya Bentlage, Gillan, Lynn, Morandini & Marques, 2011

Common name (s): Bonaire banded box jellyfish. Global distribution: Dutch Caribbean islands (then part of the Netherlands Antilles); off the shores of Mexico, St Lucia, Curacao, Barbados, Honduras and St Vincent. Ecology: It is found in shallow (less than 10 m) near-shore waters. Biology Description: Bell of this species is translucent and is densely covered in conspic- uously raised nematocyst warts. Pedalia are covered with nematocyst warts, both on outer keel and on inner wing; and pedalial wing is scalpel-shaped. Pedalial canal bend is with prominent spike. Tentacles which are flared at their bases have characteristic bands, red or orange to brown. Perradial gonads are leaf-like sheets. Stomach is extending to about 1/3 of bell height into subumbrellar cavity; and stomach is attached to subumbrella with four well-developed mesenterial bands. Manubrium is cruciform, without nematocyst warts; and lips are of square shape with nematocyst warts and smooth edges. Food and feeding: It feeds on small crustaceans and fish. Envenomation: This species has a potent sting and is highly venomous. Its sting has led to intense pain, skin damage and, in one of the cases, hospitalization. Caution is therefore advised when dealing with this species (Anon. https://en.wikipedia.org/ wiki/Tamoya_ohboya). 166 5 Biology and Ecology of the Venomous Marine Box Jellyfish (Class Cubozoa)

Collins et al. (2011) reported that the body and tentacles of this species inﬂict a serious sting. It caused intense burning, necrosis and permanent scarring of the affected skin in an adult male victim in south-eastern Brazil. The victim was hospitalized and sedated, and burning and itching persisted for 1 week.

5.8 Family Tripedaliidae

Copula sivickisi (Stiasny, 1926) ( ¼ Carybdea sivickisi)

Common name (s): Box jellyfish Global distribution: Pacific Ocean and one Indian Ocean location (the west coast of Sumatra); its range extends from Japan and Taiwan to the Philippines, Vietnam and Thailand, northern Australia, New Zealand, Micronesia and Hawaii. Ecology: It occurs in shallow warm waters. It is nocturnal and hides during the day. Biology Description: It is a very small species of jellyfish, and the medusa is growing to a size of about 10 mm in diameter. Bell is more “boxy”. Its eight gonads can be seen inside the transparent bell. In males these are orange hemispherical structures near the apex of the bell, and in females they are white-speckled, leaf-like structures. There is a central manubrium, which is a transparent tubular structure hanging down from the centre of the underside of the bell, and there are four slender tentacles 5.8 Family Tripedaliidae 167 hanging from the rim, each banded with orange. In mature females, the edge of the bell is patterned with orange-brown markings. This species has 24 eyes grouped on four-stalked rhopalia situated on the rim of the bell. Size of the specimens ranged from 1.2 to 3.2 mm in height and from 0.8 to 1.8 mm in diameter. Food and feeding: It feeds on zooplankton including phosphorescent organisms. Typical prey items include copepods, hooded shrimps, zoea larvae and the biolumi nescent dinoflagellate Noctiluca. Its typical feeding mechanism is to rise to the surface and then sink through the water with its tentacles extended to catch prey. Life cycle: This sexually dimorphic cubozoan is best known for its unique courtship behaviour and internal fertilization. Mature adults engage in courtship during which spermatophores are transferred from the male to the female, who then inserts the gametes into her manubrium. Females accept multiple spermatophores from multiple males, and only produced one embryo strand. Envenomation: Anon. (https://animaldiversity.org/accounts/Carybdea_sivickisi/) reported that the cnidocytes can be harmful to humans, if they are stung. However, the stings are not known to be fatal for humans. Anon. (https://www.pressreader.com/) reported that on contact, the stinging nematocysts of this jellyfish may leave a nasty wound that feels like a fever blister, and the blister recurs intermittently for many years.

Tripedalia cystophora Conant, 1897 168 5 Biology and Ecology of the Venomous Marine Box Jellyfish (Class Cubozoa)

Image credit: Wikimedia Commons Common name (s): Mangrove box jellyfish Global distribution: It is native to the Caribbean Sea and the Central Indo-Pacific. Ecology: It is inhabiting in shallow, muddy waters of mangrove swamps. During the day this species is mostly found within 20 cm of the surface, in sunlit positions among the prop roots of mangroves. Biology Description: Medusa of this species is about 1 cm in diameter. Its boxy dome- shaped bell has a flattened top and is slightly wider than its height. From a single point on each of the four corners of the bell arise three tentacles, each on a pedalium or stalk. Outer surface of the bell is granulated with small wart-like structures armed with nematocysts. There are four rhopalia, cylindrical structures containing light- sensitive cells. Its four flattened gonads can be seen on the inside of the bell. Underside of the bell is partially constricted by a velarium. In the centre there is a manubrium, a tube-like structure which hangs down with the mouth at its tip. This box jellyfish is translucent and yellowish brown in colour. Food and feeding: It preys mainly on copepods (e.g. Oithano nana). Life cycle: Each individual medusa of this species is gonochoristic (either male or female) and produces gametes. After fertilization, the zygote develops into a planula larva which is brooded by the female inside the bell. It is later expelled and settles to the bottom where it undergoes metamorphosis into a polyp about 1 mm long with four, knob-tipped tentacles surrounding a mouth. This may produce further polyps by budding. The oral end of each polyp differentiates into a proto-medusa which detaches itself from the base of the polyp to become a juvenile medusa. Envenomation: This tiny box jellyfish is highly venomous (Anon. https://sites. google.com/site/venomousdangerous/jellyfish/the-most-venomous-jellyfish). Biology and Ecology of the Venomous Marine Anthozoans (Class Anthozoa) 6

6.1 Family Acroporidae

Acropora digitifera (Dana, 1846)

Image credit: MDC Seamarc Maldives, Wikipedia Common name (s): Stony coral Global distribution: Tropical; Gulf of Aden, Red Sea, south-west and northern Indian Ocean, Australia, south-east Asia, central Indo-Paciﬁc, Japan, west Paciﬁc Ocean and East China Sea. Ecology: It is found in shallow reef environment sheltered from strong currents or wave action from depths of 0 to 12 m. Biology Description: Colonies of this species are digitate. Branches are 1 cm in diameter up to 10 cm long, cylindrical and slightly tapered branches. Sub-branching is

# Springer Nature Singapore Pte Ltd. 2020 169 R. Santhanam, Biology and Ecology of Venomous Marine Cnidarians, https://doi.org/10.1007/978-981-15-1603-0_6 170 6 Biology and Ecology of the Venomous Marine Anthozoans (Class Anthozoa) possible. Colonies are generally 30 cm in diameter but can reach up to 1 m. Colonies are often light brown cream with pale to dark blue tips. Black spot can be found between corallites. Polyps are brown. Axial corallites are blue or white; and relatively small tubular corallites ranging from 2 to 4 mm. Radial corallites are about 1 mm in diameter, tubular- to pocket-shaped with sharp edge. Envenomation: It is a venomous species due to its toxic proteome of nematocysts (Gacesa et al. 2015).

Acropora millepora (Ehrenberg, 1834)

Image credit: Wikipedia Common name (s): Staghorn coral Global distribution: Western and central Indo-Pacific: extends from the Red Sea, Kenya and South Africa to India, Malaysia, Japan, Indonesia and Australia. Ecology: This coral grows in shallow waters between 2 and 12 m deep; mostly on reef flats, but also on upper reef slopes and in lagoons. Biology Description: It is a small colonial, reef-building hard coral that grows in clumps. Its short branches are cylindrical. Radial corallites are all the same size and have projecting lower rims, giving them a scale-like appearance. Colour is variable and may be green with orange-tipped branches, or pale pink, orange, plain green or blue. This species grows mostly vertically, which leads to a bushy morphology that is semi-erect. Polyps extend from vertical branch tips. Polyps are on average about 1–2 mm in diameter. Food and feeding: Its main carbon requirements are fulfilled by its symbiotic dinoflagellates such as zooxanthellae which line the gastrovascular cavity of corals and contribute their photosynthetic products to the coral. However, many studies have shown that hermatypic corals are able to capture and ingest particulate food materials including phytoplankton, zooplankton and bacteria. Usually, this species extends its polyps during both the day and night. 6.1 Family Acroporidae 171

Predators: Acanthaster planci, the crown-of-thorns starﬁsh. Life cycle: It can reproduce sexually in an event called “mass spawning” which occurs once a year, around three nights in early summer during full moon time. Large quantities of eggs and sperm are released simultaneously from the huge numbers of colonies. Envenomation: Ben-Ari et al. (2018) reported that this species contains small cysteine-rich peptide toxins.

Acropora palmata (Lamarck, 1816)

Image credit: NOAA’s Florida Keys National Marine Sanctuary, Wikimedia Commons Common name (s): Elkhorn coral Global distribution: Throughout Florida Keys, Bahamas and Caribbean islands, including U.S. Virgin Islands and Puerto Rico. Ecology: It lives in shallow saltwater seas at depths ranging from 0 to 33 m. It grows typically in water temperatures from 66 to 80 F. Biology Description: It has a long, branching shape which resembles elk antlers and is spanning up to 1.5 m in diameter. This species of coral has a three-dimensional structure that is highly complex, with thick branches that are characteristic of the elkhorn coral. These elkhorn corals are cream to brownish yellow in colour, with pale cream to white branch tips. This species may grow to a height of 3 m in reef areas that are exposed to strong waves. Food and feeding: Acroporids host symbiotic algae called zooxanthellae. While this species gets most of their nutrients from the by-products of the algae’s photosynthesis, they also have barbed, venomous tentacles, and they can stick out to grab zooplankton and even small ﬁsh. 172 6 Biology and Ecology of the Venomous Marine Anthozoans (Class Anthozoa)

Life cycle: The dominant mode of reproduction for acroporids is asexual fragmentation, in which branches break off and reattach to the substrate to form new colonies. Individual colonies are hermaphrodites (both male and female reproductive organs in a single individual). Once a year, in late summer, sexual reproduction occurs via the release of millions of reproductive cells into the water. Polyps and the reefs they form can live for hundreds of years. Envenomation: This venomous species releases nematocysts that are venomous when touched, as a tactile response which can cause paralysis (Blaxter et al. 1984; Anon. https://sta.uwi.edu/fst/lifesciences/sites/default/ﬁles/lifesciences/images/ Acropora%20palmata%20-%20Elkhorn%20Coral.pdf).

Astreopora sp.

Image Credit: Wikipedia Commons Common name (s): Star coral Global distribution: Red Sea, Indian Ocean and western Paciﬁc. Ecology: It is found in a range of environments including shallow or muddy waters, as well as deeper areas of the reef where plating forms are most common. Biology Description: Members of this genus mostly form dome-shaped or rounded heads but sometimes have leaf-like extensions which may encrusting, plates, vases or branches These species are much larger than members of the genus Montipora. They have a wide range of colours including yellow, brown, green, pink and blue, but the most common are whitish-blue. Corallites are distinct and separate, sometimes raised on cones and sometimes depressed, up to 4 mm across. Skeleton is porous with the coenosteum having a net-like appearance. This coral species appears rough-textured because of tiny spines that cover the surface between the corallites. Septa are poorly developed, giving corals of this genus the appearance of being ﬁlled with holes. 6.2 Family Actiniidae 173

Envenomation: Injuries caused by this venomous stony coral are mostly external in nature. Minor cuts and grazes are easily caused by its sharp-edged calcium carbonate skeleton. Such injuries can be very painful, as toxic secretions from nematocysts enter the wound when the injury occurs (Blaxter et al. 1984; Anon. https://www.vapaguide.info/catalogue/CNI-147).

6.2 Family Actiniidae

Actinia australiensis Carlgren, 1950

Common name (s): Australian anemone Global distribution: Eastern Australia. Ecology: The individuals of this species are seen on undersurface of rock and dead oyster shell. Biology Description: Not reported Envenomation: The peptide and protein toxins of this species may be harmful. This species has been largely unexplored for its toxin contents and is currently under investigation to identify new peptide and protein toxins with potentially novel functions (Prentis et al. 2018). 174 6 Biology and Ecology of the Venomous Marine Anthozoans (Class Anthozoa)

Actinia bermudensis (McMurrich,1889)

Common name (s): Red, maroon or stinging anemone Global distribution: Throughout the tropical Atlantic Ocean: from Brazil to Florida and Bermuda. Ecology: It is found in the intertidal and the sublittoral zone near the base of rock walls, under overhangs, in caves, in crevices and under boulders, also in estuaries. Biology Description: It attaches itself to a rock surface by its pedal disc, which can reach 2.5 cm in width. Column is narrower at the top than the base and can reach 5 cm in height. Near the top is a ring of bulges called acrorhagi which contain many cnidocytes. Its oral disc has a central mouth and two irregular whorls of 96–140 short, retractable, tapering tentacles which are armed with cnidocytes. Colour of the anemone is dark red or maroon; and acrorhagi are blue or pink. Food and feeding: It is an omnivore and its main items of prey are gastropods, isopods and small bivalves. Other food items may include other marine invertebrates and algae. Predators: Life cycle: In this species, reproduction can take place by fission in which the anemone is splitting in half longitudinally. Alternatively, sexual reproduction occurs, with internal fertilization. In this case, the juvenile sea anemones are brooded by the parent in the gastrovascular cavity until they have grown sufficiently large to be released into the water column. Another method of reproduction is a form of parthenogenesis in which the young are brooded internally. Association: Like other sea anemones, this species may also form symbiotic relationships with photosynthetic dinoflagellates, called zooxanthellae. Envenomation: Yamaguchi et al. (2010) reported on the presence of Kv1 potassium channel toxins in this species. Orts et al. (2018) reported on the isolation of a 6.2 Family Actiniidae 175 peptide, called AbeTx1 which yielded 12 different subtypes of KV channels (KV1.1–KV1.6; KV2.1; KV3.1; KV4.2; KV4.3; KV11.1; and Shaker IR) and three voltage-gated sodium channel isoforms (NaV1.2, NaV1.4 and BgNaV) on purification.

Actinia cari Delle Chiaje, 1822

Common name (s): Girdle anemone Global distribution: Subtropical Mediterranean Sea and Atlantic Ocean. Ecology: This solitary, sessile species is found on the rocks of surface to a few metres of depth from infralittoral and subtidal zones. Biology Description: This species grows to approximately 4–5 cm in width and 8 cm in height. It can fully retract its tentacles. It has a brown-green to reddish colour, with concentric, dark, longitudinal rings on the body wall. It is roughly cylindrical to conical in shape. Food and feeding: This is a nocturnal species catching small prey with its tentacles. Envenomation: This sea anemone contains three caritoxins viz. CTX, CTX II and CTX III which are lethal and haemolytic polypeptides (Sencic and Macek 1990; Anon. https://en.wikipedia.org/wiki/Actinia_cari). Anderluh and Macek (2012) reported that the cytolytic peptide and protein toxins of this species possessed lethality and pore formation activity. 176 6 Biology and Ecology of the Venomous Marine Anthozoans (Class Anthozoa)

Actinia equina (Linnaeus, 1758)

Image credit: Wikimedia Commons Common name (s): Beadlet anemone Global distribution: It is common in British Isles. Its range extends to the rest of Western Europe and the Mediterranean Sea, and along the Atlantic coast of Africa as far south as South Africa. Ecology: It is found on rocky shores at depths of around 20 m; and in exposed and sheltered situations. It is highly adapted to the intertidal zone as it can tolerate both high temperatures and desiccation. The anemone may also be found in regions of variable salinity such as estuaries. Biology Description: It has a broad base which is up to 5 cm in diameter and is usually wider than tall. Column is smooth. There are up to 192 retractable tentacles which are arranged into six circles. Bright blue wart-like spots called acrorhagi are often found round the inside of the top margin of the column. Animals are red, green, brown or orange in colour (Ager 2008). Life cycle: It is viviparous, with up to 100 embryos developing inside the body cavity before being ejected into the open water as juveniles. Envenomation: It stings the victim with its nematocysts (Anon. https://www. marlin.ac.uk/species/detail/1561). Sket et al. (1974) reported on the occurrence of equinatoxin, a lethal protein, from this species. Macek and Lebez reported on the presence of equinatoxins I, II and III with lethal potency from this species. Shiomi et al. (1997) and Frazão et al. (2012) reported on the presence of sodium channel toxin and KV channel toxin (AeK) in this species. These toxins are believed to be responsible for heart failure. Anderluh and Macek (2012) reported on the presence of cytolytic peptide and protein toxins (cytolysins), with pore formation activity. Anon. (http://www.thecephalopodpage. org/MarineInvertebrateZoology/Actiniabermudensis.html) reported on the presence of various lethal toxins manufactured by this species. 6.2 Family Actiniidae 177

Prentis et al. (2018) reported that most injuries caused by this species are associated with skin rashes and oedema. Further, a swimmer lost consciousness and underwent cardiopulmonary arrest after being stung by this sea anemone.

Actinia fragacea Tugwell, 1856 Image not available Common name (s): Strawberry anemone Global distribution: Temperate north-east Atlantic: from Norway to Africa, including adjacent islands (Azores, Canary Islands and Cape Verde) and the Mediterranean. Ecology: Intertidal zone; this reef-associated species is generally found on rocks of the lower shoreline and sublittoral zone at depths up to 10 m; sometimes it is found partly buried in sand. Biology Description: It is a large anemone with a broad base (up to 10 cm across). Column is red, ranging from bright scarlet to deep brownish crimson, and is covered with small green spots. Spots give this anemone its common name as they look like strawberry pips. Wart-like spots (acrorhagi), to which gravel and stones attach, may be present. Tentacles are usually red or purplish. Life cycle: Little is known of the reproduction of this species, but it has separate sexes and has an oviparous system of reproduction. It does not seem to brood its young. Envenomation: Its venom contains a toxin (cytolysin) named fragaceatoxin C (FraC) which possesses haemolytic activity (Imani et al. 2017; Bellomio et al. 2009; Frazão et al. 2012).

Actinia tenebrosa Farquhar, 1898 178 6 Biology and Ecology of the Venomous Marine Anthozoans (Class Anthozoa)

Image credit: John Turnbull, Wikipedia Common name (s): Waratah anemone Global distribution: Tropical southern Australia, from Perth to New South Wales, New Zealand. Ecology: It is a mid intertidal species and is found relatively high on the seashore, in rock pools and shaded surfaces such as under rock overhangs. Biology Description: This species is a solitary polyp that lacks the medusa stage. In underwater, this sea anemone opens up to display numerous tentacles, arranged in three whorls. Out of water, these tentacles retract and the anemone seems to resemble a dome-shaped red, crimson, brown, green or black blob of jelly, about 4 cm across and 2.7 cm high. When it is well exposed to the rays of the sun, its column is greenish or brownish black, and the disc and tentacles are in dusky crimson, while those on the undersides of overhanging stones are reddish brown or crimson. Intensity of its colour is varying according to the amount of light which reaches the animal. Its column has a number of iridescent blue spherules armed with nematocysts. Food and feeding: It is an opportunistic feeder on fishes, shrimps, worms. It displays intraspecific aggressive behaviours during contest for space. Predators: Life cycle: This species is viviparous and broods its young inside its body cavity. When the offspring are well-developed, they are expelled through the mouth. The juveniles often attach to rocks. It can also reproduce sexually with planktonic larvae which are settling far away from the parent individual. Envenomation: Its protein toxin, tenebrosin-A, causes cardiac stimulation and haemolysis in guinea pig erythrocytes. Further, it is reported that this toxin exerts a strong positive inotropic effect on isolated guinea pig atria at a concentration of 1.4 nM, with little chronotropic activity (Thomson et al. 1987). Further, this cytolytic peptide possesses pore formation activity (Anderluh and Macek 2012). According to Frazão et al. (2012), this species contains the protein toxins, tenebrosins A, B and C. Anon. (https://www.gbri.org.au/Species/Actiniatenebrosa.aspx?PageContentID¼ 1484) reported that on contact with the victim, its acrorhagi (wart) becomes inflated discharging nematocysts. This causes necrotic lesions on the epidermis of the victim. 6.2 Family Actiniidae 179

Anemonia erythraea (Hemprich & Ehrenberg in Ehrenberg,1834)

No information on the Biology and Ecology of this species is available. Envenomation: This species has been reported to contain three polypeptide toxins AETX I, II and III which caused crab lethality. Further its haemolysins possess haemolytic activity (Shiomi et al. 1997; Rodríguez et al. 2018; Frazão et al. 2012).

Anemonia sulcata Pennant, 1777

Common name (s): Snakelocks sea anemone Global distribution: Subtropical Mediterranean Sea. 180 6 Biology and Ecology of the Venomous Marine Anthozoans (Class Anthozoa)

Ecology: This solitary sea anemone is found hanging on walls that are exposed to the sun’s rays or in rocky areas down to a depth of 5 m. It retreats in crevices when currents are strong. Biology Description: This sea anemone presents two forms which relate to its two living distinct biotopes, called ecotypes. Forms of ecotype I possess 70–192 tentacles and their pedal disc has a diameter from 2 to 5 cm. On the other hand, the forms of ecotype II showed a maximum of 348 tentacles, with a pedal disc of 15 cm in diameter. At these two ecotypes, tentacles of these sea anemones have a size of about 20 cm and are very fine and mobile, but not very contractile. They are laid out in six concentric crowns around the siphonoglyph and are thinned gradually. Colourings of these two types of sea anemones are conditioned by the presence or the absence of symbiotic algae, and are white with the tone greens. Their end frequently raises a bulge of colour violet. Life cycle: The reproduction system of these sea anemones is simple, and they have no true gonads or special ducts for the emission of the gametes, which enter the gastrovascular cavity breaking through the mesenterial epithelium. They have both sexual and asexual reproduction. During the sexual reproduction, germ cells arise in the mesenterial gastrodermal layer and migrate to the mesoglea, where their maturation takes place. Envenomation: Ecotype I organisms are found equipped with a powerful irritant capacity, incompetent however to be exerted through the thick skin of the end of the fingers. On the other hand, anemones of ecotype II may prick the face, the neck, the interior of the arms or others. The open wounds of the hands may also be significant points (Anon. https://www.sealifebase.ca/summary/Anemonia-sulcata.html). This sea anemone was the clinically most important one in the Adriatic Sea. Between 1965 and 1980, 55 patients stung by this cnidarian were seen at the Pula Medical Center in Istria, Yugoslavia. The majority of injuries were inflicted upon the upper extremities, chest or abdomen. Pain and the appearance of small blanched papules surrounded by slightly reddened and oedematous bases were the initiating manifestations. Linear lesions were sometimes seen. Resulting vesicles were found filled with serous fluid, localized discolouration, and the formation of bullae sometimes followed. Somnolence, dizziness, nausea, vomiting, muscle aches and lid oedema were reported in some cases (Maretić and Russell 1983; Prentis et al. 2018). Anon. (https://www.uniprot.org/uniprot/P01529) and (https://www.uniprot.org/ uniprot/Q9TWG1) reported on the presence of two toxins viz. Delta-AITX-Avd1d and Kappa-AITX-Avd6a from this species. 6.2 Family Actiniidae 181

Anemonia viridis Forskal, 1775

Image credit: Obra do próprio, Wikipedia Common name (s): Snakelocks anemone Global distribution: Adriatic; southern and western shores of Britain and as far south as the Mediterranean Sea. Ecology: It is living in shallow waters and rocky pools. It requires high intensity light levels. Biology Description: Size of this species is up to about 70 mm across the base with a tentacle span of up to 180 mm. Base is lightly but closely adherent and is broader than column. Column is variable in height and is often short and hidden by the tentacles. It is smooth with small, roughly conical acrorhagi on the parapet. Disc is wide. Tentacles which are up to about 200 in number are long, fairly stout and flexuous. They are rarely retracted. Column of the anemone is reddish or greyish brown; usually darkest above and sometimes with irregular pale streaks. Acrorhagi are matching the ground colour. Disc is brown or greyish, usually with white radial lines. Tentacles are grey-brown or bright grass green with purple tips. Some tentacles may, however, bear a median longitudinal pale line. Food and feeding: Tissues of this species contain zooxanthellae (symbiotic algae) which appears to be necessary for the long-term survival of this sea anemone. It ingests larger food items both dead and alive, e.g. small fish and just moulted palaemonid prawns. Gastropod molluscs and all sorts of crustaceans form the bulk of the diet of this species. Life cycle: This species reproduces with asexual method. By longitudinal fission, this anemone splits into two identical halves. This process can take from 5 min to 2 h. Envenomation: Frazão et al. (2012) reported on the presence of NaV channel toxins, ATX-I, II, III and V; and KV channel toxins, SA5 II, kalicludins-1,2,3, BDS-I, II and kaliseptin from this species. 182 6 Biology and Ecology of the Venomous Marine Anthozoans (Class Anthozoa)

Small children playing in the rocky pools are especially prone to the tentacle envenomation of this species since their skin and mucosa are more tender. The affected area of the skin takes on a reddened and slightly raised appearance, bearing irregularly scattered pin-head size vesicles and sometimes an oedema may develop around the injured skin. On lips and child skin larger blisters can also develop. The area becomes painful, particularly to touch and heat (Turk 1999).

Antheopsis maculata Simon, 1892

Common name (s): Sea anemone Global distribution: Philippines. Ecology: It occurs at a depth of 31 m Biology Description: The taxonomy of this species is questionable. Envenomation: Three peptide toxins (Am I, II, III) with crab toxicity have been isolated from this species (Honma et al. 2005). Frazão et al. (2012) and Rodríguez et al. (2018) reported on the presence of NaV channel toxin, Am-3; KV channel toxin, Am-2; and an ungrouped peptide toxin, Am-1, with crab toxicity. 6.2 Family Actiniidae 183

Anthopleura asiatica Uchida & Muramatsu, 1958

Common name (s): Sea anemone Global distribution: Pacific and Japan Sea; Honshu to Kyushu. Ecology: It is an intertidal, coastal species. Biology Description: This species is generally columnar and it reaches 20–25 mm height and 15–20 mm width or 15–20 mm height and 20–25 mm width. Column is liable to be flaccid. Tentacles and oral disc are greyish brown. Column is greyish green, with many small reddish-brown warts arranged in 48 vertical rows. Of these rows, 12 are comparatively distinct, corresponding to the tentacles of the first and second series; and others correspond to the other tentacles. Tentacles are 48 in number and are arranged in the formula 6:6:12:24. In larger individuals, acrorhagi (warts) are found. Mesenteries are 48 pairs which are divided into 12 primary, 12 secondary and 24 tertiary cycles. Only the primary 12 mesenteries are, however, perfect. Envenomation: The crude venom of this species was found to be lethal at 1 mL when injected intra-peritoneal to Kasauli strain male albino mice. The symptoms of toxicity observed in the mice indicated that the venom affected the central nervous, cardiovascular and urinary systems (Ramkumar et al. 2012). Frazão et al. (2012) reported on the presence of a cytolysin bandaporin from this species. 184 6 Biology and Ecology of the Venomous Marine Anthozoans (Class Anthozoa)

Anthopleura dowii Verrill (1869)

Image credit: Arizona-Sonora Desert Museum Common name (s): Mexican anemone Global distribution: Tropical eastern central Paciﬁc. Ecology: It is a demersal species. Biology Description: Not reported Food and feeding: It feeds on brine shrimp nauplii, brine shrimps, copepods, cladocerans and mysids. Envenomation: Ramírez-Carreto et al. (2019) reported that the pore-forming protein of the venom of this species showed haemolytic activity in the human erythrocytes. 6.2 Family Actiniidae 185

Anthopleura elegantissima (Brandt, 1835)

Image credit: Davefoc, Wikipedia Common name (s): Clonal anemone, green aggregating anemone Global distribution: Pacific coast of North America: from Alaska to Baja California. Ecology: It is found either in dense populations or solitary, on rock walls, boulders or pilings from between high- and low-tide lines to low-tide line. It, however, prefers to live in semiprotected areas near the outer coast. Biology Description: Polyps of this aggregating anemone can be up to 6 cm high on their column and 8 cm wide. It is cylindrical and its column is pale grey-green to white. Most specimens are olive to bright green (depending on the species of algal symbionts present) with tentacles tipped in pink. Individuals that live under docks or in caves lack symbionts and are pale yellow to white in colour. Tentacles are variously coloured, with pink, lavender or blue tips, and are arranged in five rings around oral disk. This species has a ring of white knobs, called acrorhagia, just outside their ring of tentacles. These acrorhagia are loaded with stinging cells and are used for fighting other anemones. Column is covered with vertical rows of adhesive tubercles called verrucae. This cnidarian hosts endosymbiotic algae called zooxanthellae that contributes substantially to primary productivity in the intertidal zone. Predators: Nudibranch (Aeolidia papillosa), leather star, Dermasterias imbricata and mosshead sculpin, Clinocottus globiceps. Life cycle: This species is capable of reproducing both sexually and asexually. As adults, these aggregating anemones release gametes into the water that unite to form genetically unique individuals that settle on intertidal rock. This genetically distinct individual can then proliferate through binary fission. According to some scientists, 186 6 Biology and Ecology of the Venomous Marine Anthozoans (Class Anthozoa) this is not true reproduction but actually a form of growth. The asexual method, fission, follows the sexual spawning in summer. Over time, a single individual can generate a large colony of genetically identical polyps. Association: This anemone may harbour either zooxanthellae (dinoflagellate) or zoochlorellae (chlorophyte) intracellular symbionts. In California, the zooxanthellae may be either Symbiodinium californium or S. muscatinei. In Oregon and Washington the only zooxanthellae symbionts belong to the species S. muscatinei. Envenomation: The venom of this species contains NaV channel toxins, viz. anthopleurin-C, APE 1-1, APE 1-2, APE 2-1 and APE 2-2; and Kv toxins APET x1 and APET x2 (Frazão et al. 2012). Diochot et al. (2003) reported that a new peptide, APETx1, which specifically inhibits human ether-a-go-go-related gene (HERG) potassium channels, was purified from the venom of this species. Bruhn et al. (2001) reported on the presence of five toxins (APE 1 to APE 5) from the venom of this species. Among them, APE 2-1 was found to be most potent cardiotoxic isotoxin.

Anthopleura fuscoviridis Carlgren, 1949

Image credit: Canon EOS 5D Mark II Common name (s): Rainbow bottom anemone, Japanese green ﬂower Global distribution: Subtropical species; Japan. Ecology: It is a shallow water species and it attaches itself between the sand and the cracks in the rocks at depths of 3–4m. Biology Description: Tentacles of this species are often pink, but there is some variation in colour as well. Colour of the body varies as well, but it has distinct bright green warts on the body wall. 6.2 Family Actiniidae 187

Envenomation: Anderluh and Macek (2012) reported that this species has cytolytic peptide and protein toxins (cytolysins). Sunahara et al. (1987) reported on the presence of two toxins, AFT-I and AFT-II, from this species. Frazão et al. (2012) reported on the presence of two NaV channel toxins, AFT-I and AFT-2, from this species. Anon. (https://www.uniprot.org/uniprot/P0DMJ3) and (https://www.uniprot.org/ uniprot/P10454) reported on the presence of PI-actitoxin, Afv2a and Delta-actitoxin, Afv1b from this species.

Anthopleura japonica Verrill, 1899 (¼ Gyractis japonica; Anthopleura kurogane)

Common name (s): Sea anemone Global distribution: Tropical; north-west Paciﬁc; middle to the northern coasts of Japan. Ecology: It dwells in crevices of rock under the tidal line and is buried in sand, bearing pebbles on its upper part. Biology Description: Warts of the column of this species are thickly distributed only on the upper half of the body. Tentacles are greyish brown, usually with white spots and sometimes slightly pink coloured. Oral disc is greyish brown. Column is greyish brown in the upper portion and yellowish brown, ﬂesh colour or bluish in the lower part. Acrorhagi are clearly seen in young individuals but gradually disappear in large ones. Envenomation: Anderluh and Macek (2012) reported on the occurrence of cytolytic peptide and protein toxins in this species. Shiomi et al. (1986) reported on the presence of lethal haemolysin in this species. 188 6 Biology and Ecology of the Venomous Marine Anthozoans (Class Anthozoa)

Anthopleura michaelseni (Pax, 1920)

Image credit: Seascapeza, Wikipedia Common name (s): Long-tentacled anemone, crevice anemone Global distribution: Tropical south-east Atlantic, western Indian Ocean; southern Africa between Lüderitz and Durban. Ecology: It is a sessile, very shallow water species found partially buried in sand in rock crevices, with a depth range of 5–15 m. Biology Description: It is a large anemone of up to 15 cm in diameter. Its column has large sticky pads to which sand and debris particles adhere. On the oral surface, dark stripes run from the mouth to the tentacles. It has 96 long tentacles with small round protrusions (spherules) at their base. Life cycle: It produces eggs and sperm, and the fertilized egg develops into a planula larva which drifts as part of the plankton before settling on the seabed and developing directly into a juvenile sea anemone. Envenomation: Anderluh and Macek (2012) reported on the presence of cytolytic peptide and protein toxins (cytolysins) in this species. 6.2 Family Actiniidae 189

Anthopleura xanthogrammica Brandt, 1835

Image credit: Wikimedia Commons Common name (s): Giant green anemone, green surf anemone, giant green sea anemone, green anemone, giant tidepool anemone, anemone and rough anemone. Global distribution: Pacific Ocean: from Alaska to southern California and sometimes downwards to Panama. Ecology: It occurs form low to mid intertidal zones and is inhabiting sandy or rocky shorelines, where water remains for most of the day. It can also be found in tide pools up to 15 m deep. Occasionally this species is found in deep channels of more exposed rocky shores and concrete pilings in bays and harbours. Biology Description: Column width and height of this species can reach a maximum of 17.5 and 30 cm, respectively. Its crown of tentacles can be as wide as 25 cm in diameter, while the column, itself, tends to be widest at the base. It has a broad, flat oral disk surface, and there are no striping, banding or other markings. Tentacles, which are short and conical, are arranged in six or more rows surrounding the oral disk and can be pointed or blunt at the tips. If this species is exposed to proper amounts of sunlight, it can appear bright green when submerged under water. When not submerged, it appears dark green or brown. Food and feeding: The anemone feeds on sea urchins, small fish and crabs, but detached mussels seem to be the main food source. Nematocysts found in its tentacle species assist in catching and paralysing prey. After feeding and digestion is complete, the anemone excretes its waste back through the mouth opening. Predators: Main predators of this species include the leather seastar, Dermasterias imbricata, the nudibranch Aeolidia papillosa and the snail Epitonium tinctum (both feed on the tentacles), and the snails Opalia chacei and Opalia funiculata and the sea spider Pycnogonum stearnsi (that feed on the column). Life cycle: It reproduces sexually via external fertilization of sperm and eggs. Newly formed planktotrophic larvae float in the water until they settle in mussel beds. 190 6 Biology and Ecology of the Venomous Marine Anthozoans (Class Anthozoa)

Association: Photosynthetic, symbiotic algae, zoochlorellae and the dinoflagellates, zooxanthellae, live in the epidermis and tissue of the gut of this species. Envenomation: Its stinging cells located in the tentacles are harmful (Anon. https://en.wikipedia.org/wiki/Anthopleura_xanthogrammica). Anderluh and Macek (2012) reported on the presence of cytolytic peptide and protein toxins (cytolysins) in this species. Frazão et al. (2012) reported on the presence of NaV channel toxins, anthopleurins A, B and toxins PCR1 to Toxin PCR7; and Kv channel toxin AXPI- I in this species. Anon. (https://www.uniprot.org/uniprot/P0C5F8) reported on the occurrence of the toxin delta-actitoxin-Axm1c in this species. This toxin is known to weakly inhibit voltage-gated sodium channels. Anon. (https://www.uniprot.org/uniprot/P0C5F9) reported on the presence of the toxin delta-actitoxin-Axm1e in this species. This toxin binds specifically to voltage- gated sodium channels (Nav), thereby delaying their inactivation. Kelso and Blumenthal (1998) reported on the presence of neurotoxins, 49 residue toxins, in this species. These toxins interact with the sodium channel with even higher affinity, enhancing sodium uptake.

Arctapodema sp. Envenomation: Extracts of this unidentiﬁed species showed haemolytic activity and caused cytolysis (Mariottini 2014). Sunahara et al. (1987) reported on the presence of toxins anthopleurins A and B from this species. Frazão et al. (2012) reported on the presence of NaV channel toxins Hk16, Hk2, Hk7 and Hk8 in this species.

Aulactinia marplatensis (Zamponi, 1977) (¼ Bunodactis marplatensis)

Common name (s): Not designated Global distribution: Argentina. 6.2 Family Actiniidae 191

Ecology: It lives in the rocky intertidal areas. Biology Description: Column of this species is cylindrical, taller than wide and its diameter is 2.5–4.5 cm. It is greenish brown, with darker regularly placed adhesive verrucae, arranged in 48 longitudinal rows that run the entire length of the column. Verrucae are with red centre in some live specimens and are colourless after preservation. Oral disc is ﬂat, and mouth is central. Regularly spaced pale lines are radiating from margin in some specimens. Tentacles (76–92) are white, pinkish or purple and are distributed in four cycles. Pedal disc is well developed and is more or less circular. Envenomation: Anderluh and Macek (2012) reported on the presence of cytolytic peptide and protein toxins (cytolysins) in this species.

Aulactinia veratra (Drayton in Dana, 1846)

Image credit: David Staples Common name (s): Green snakelock anemone Global distribution: South-eastern Indian Ocean and south-western Paciﬁc Ocean; west, south and east coasts of Australia, Tasmania and both islands of New Zealand. Ecology: It is found in the intertidal zone in rock pools, under overhangs, between boulders, and in crevices. The base is ﬁrmly attached to a rocky substrate. Biology 192 6 Biology and Ecology of the Venomous Marine Anthozoans (Class Anthozoa)

Description: This green snakelock anemone reaches a maximum height of 60 mm when it is fully extended. Its broad column has rows of verrucae (wart-like outgrowths) on its surface to which coarse grains of sand and fragments of shell adhere. Oral disc has a central mouth surrounded by a whorl of long, tapering tentacles (24–124) with blunt tips. When expanded, both the column and tentacles of this anemone are usually green, but brown or red individuals sometimes occur. When retracted, with the oral disc and tentacles tucked inside the body cavity, green individuals may appear black. Envenomation: Prentis et al. (2018) reported on the occurrence of new peptide and protein toxins with potentially novel functions.

Bolocera tuediae Johnston, 1832

Common name (s): Deeplet sea anemone Global distribution: Subtropical and temperate; Atlantic: North Sea, USA and Canada; Newfoundland, British and Irish coasts. Ecology: This sessile anemone is found from depths of 50 to 100 m in the sublittoral zone; and closed off marine areas attached to hard substances such as stones, rocks and shells. Description: It is one of the largest of the North Sea anemones and is up to 250 mm across the base. Base is lightly adherent. Column is cylindrical and is variable in height; sometimes taller than wide but often kept short and hidden by the tentacles, smooth and soft in texture, never with verrucae or acrorhagi, and is occasionally with a slight rim at the top. Disc is wide. Tentacles are stout, long and is not readily retracted; and they are hexamerously arranged, up to about 200. Animal is fairly uniform—orange, buff, pink or whitish; and disc and tentacles are slightly translucent. Disc is sometimes with vague indications of a dark pattern around the tentacle bases. Life cycle: These anemones have their largest gonads (sex glands). The females have pink, spherical eggs with a membrane. When its nucleus is fertilized, it will make several daughter nuclei. Each nucleus will spread until they are evenly 6.2 Family Actiniidae 193 distributed. As the eggs mature, they will undergo segmentation and become blastula which will flatten and sink downwards. The gastrula formed is made up of three layers. About 25 days after the eggs have been shed, fixation will occur. The base will form the shape of a disc and grow; the mouth opens and the larvae shorten. Finally the anemones become largely dormant. Association: The deeplet sea anemone was observed to have a symbiotic relationship with shrimp. Envenomation: The nematocysts of this anemone can have dangerous effects, including the rupturing of human blood cells. Venom from both the cell membranes and tentacles alike have these effects, but venom from membranes causes cell death in skin, blistering and can cause blood to coagulate. Further, these anemones have two polypeptides, viz. BTTX I and BTTX II, that are able to paralyse crabs. Further, BTTX II can interfere with the inactivation and activation of sodium channels in the muscle membrane of rats (Tesseraux et al. 1989; Shiomi et al. 1997; Anon. https:// en.wikipedia.org/wiki/Bolocera_tuediae). Anderluh and Macek (2012) identified cytolytic peptide and protein toxins (cytolysins) from this species. Nematocyst venoms from the mesenteric filament and tentacles of this species contain toxins capable of killing mice and haemolysing human erythrocytes. The mesenteric filament venom is capable of accelerating clotting of whole human blood and inducing dermonecrosis and vesiculation. Both venoms contain alkaline and acid proteases as well as aminoesterases. Tentacle venom also contains AMPase, ADPase and ATPase (Calton et al. 1978).

Bunodactis reynaudi (Milne Edwards, 1857) 194 6 Biology and Ecology of the Venomous Marine Anthozoans (Class Anthozoa)

Image credit: Pbsouthwood, Wikipedia Common name (s): Sandy anemone Global distribution: Coasts of southern Africa between Luderitz and Durban. Ecology: This very shallow water species inhabits waters from the intertidal to about 4 m in depth. It is also found in pools on the lower shore and in crevices on rocks and is often huddled into sandy gullies and round the bases of boulders. Juveniles are often found in mussel beds. Biology Description: The sandy anemone is a medium-sized anemone of up to 10 cm in diameter. It has about 300 short tentacles. Its body column is covered with sticky knobs which have sand and debris particles adhered. It has a wide range of colours, including pink, brown, green and blue, often with a contrastingly coloured oral disc. Food and feeding: It feeds on mussels, whelks, other molluscs and urchins. It has an extremely strong contractile sphincter muscle which helps to grip and ingest passing food quickly. Life cycle: it produces eggs and sperm, and the fertilized egg develops into a planula larva which drifts as part of the plankton before settling on the seabed and developing directly into a juvenile sea anemone. Envenomation: Anderluh and Macek (2012) reported that this species has cytolytic peptide and protein toxins (cytolysins), in its tentacle nematocysts.

Bunodosoma caissarum Correa in Belem, 1987

No information on the Biology and Ecology of this species. Envenomation: Shiomi et al. (1997) reported on the presence of sodium channel toxin, BTTX II, from this species. Anderluh and Macek (2012) reported on the presence of cytolytic peptide and protein toxins (cytolysins) in this species. Frazão et al. (2012) reported on the presence of NaV channel toxin, Bc-III; Kv channel toxins, BcIV and BcV; and PLA2 toxins in the venom of this species. 6.2 Family Actiniidae 195

Oliveira et al. (2006) reported that the toxin BcIV of this species is a paralysing peptide. Malpezzi et al. (1993) reported on the presence of a haemolysin, bunodolysin or Bc-H from this species. Orts et al. (2013) reported on the presence of BcsTx3 (a novel sea anemone toxin family of potassium channel blocker) in this species.

Bunodosoma cangicum Belem & Preslereravo, 1973

No information on the Biology and Ecology of this species. Envenomation: Yamaguchi et al. (2010) reported on the presence of Kv1 potassium channel toxins in this species. Frazão et al. (2012) reported on the presence of NaV channel toxins, Cangitoxin, Cangitoxins 2,3; and Kv channel toxin Bcg III in this species. Lagos et al. (2001) reported on the haemolytic and neuroactive properties of the venom of this species. Anon. (https://www.uniprot.org/uniprot/P58305) reported that the injection of its granulitoxin in mice produced severe neurotoxic effects such as circular movements, aggressive behaviour, dyspnea, tonic-clonic convulsion and death. 196 6 Biology and Ecology of the Venomous Marine Anthozoans (Class Anthozoa)

Bunodosoma capensis (Lesson, 1830)

Image courtesy: Ohna Nel, courtesy Two Oceans Aquarium Common name (s): Knobbly anemone Global distribution: Tropical south-east Atlantic (from Luderitz to Durban), south-east Paciﬁc; southern African coast from Namibia to KwaZulu-Natal. Ecology: This sessile species inhabits shallow reefs in sandy free areas from the intertidal to 20 m in depth; usually found on rocky ledges; and is often found attached to mussels or red bait, Pyura stolonifera. Biology Description: Knobbly anemone is a medium-sized anemone of up to 10 cm in diameter. These anemones are very variable. They can be white, maroon, pink, red, blue, purple or orange. Their central column is lined with a series of small, usually purple, knobs that are small and more darkly coloured than the rest of the body. These knobs are not sticky, and sand and debris do not stick to the column of knobbly anemones. It has small round protrusions (spherules) at the base of its tentacles. Envenomation: A novel potassium channel inhibitor (neurotoxin) has been isolated from this species. The isolated inhibitor at 3.98 nM inhibited the potassium channels in MCF-7 cells to 70% (van Losenoord et al. 2018). Anderluh and Macek (2012) reported on the presence of cytolytic peptide and protein toxins (cytolysins) in this species. 6.2 Family Actiniidae 197

Bunodosoma granuliferum (Le Sueur, 1817)

Image credit: Hernández Albernas, Joan; WoRMS Common name (s): Red warty sea anemone Global distribution: Caribbean Sea; from Bermuda to Barbados. Ecology: It lives in shallow waters on sandy and rocky areas, and seagrass fields; also in lagoon and back-reef zones; and a depth range of 0.5–6m. Biology Description: Animals with fully expanded tentacles and oral disc are of 100 mm in diameter. Oral disc is 10–70 mm in diameter, smooth and flat and olive green or reddish brown. There are 48–96 tentacles; hexamerously arranged in four or five cycles; simple and conical; moderately long, 10–30 mm in length; smooth and tapering distally; inner ones are longer than outer ones; contractile and are olive green to green-greyish, often with white spots and flashes of pink or purple. Margin is with acrorhagi. Column is cylindrical, 6–55 mm in height and 6–38 mm in diameter, and is densely covered with rounded non-adhesive vesicles arranged in 24 alternating dark and light bands. Pedal disc is well-developed; 8–42 mm in diameter and olive green to orange. Mesenteries are hexamerously arranged in four cycles: first, second and some mesenteries of third cycle are perfect and others are imperfect. Symbiotic zooxanthellae are present. Association: This species was found adhered to a leaf of Thalassia testudinum,as epiphytic species do. It is reported to be associated with the crustaceans Periclimenes rathbunae, Thor amboinensis and some reef fishes. Envenomation: Anon. (https://www.uniprot.org/uniprot/G0W2H7) reported on the presence of a toxin, U-AITX-Bg1a in this species. This toxin potently and selectively inhibits voltage-gated potassium channels Kv11/KCNH/ERG. Yamaguchi et al. (2010) reported on the presence of potassium channel toxins κ1.3, ATTX and Bg1a (BgK) in this species. 198 6 Biology and Ecology of the Venomous Marine Anthozoans (Class Anthozoa)

A neurotoxic peptide, granulitoxin (GRX), has been isolated from this sea anemone. Puriﬁed GRX when injected into mice produced severe neurotoxic effects such as circular movements, aggressive behaviour, dyspnea, tonic-clonic convulsion and death (Santana et al. 1998). Frazão et al. (2012) reported on the presence of NaV channel neurotoxins Bg-2 and Bg-3; Kv channel toxin, Bgk; and ungrouped toxin, granulitoxin, from this species. Anon. (https://www.rcsb.org/structure/1bgk) reported that the toxin 1Bgk of this species served as potassium channel inhibitor.

Condylactis aurantiaca (Delle Chiaje, 1825)

Image credit: Esculapio, Wikipedia Common name (s): Golden anemone, golden delicious anemone Global distribution: It is found only in the Mediterranean Sea. Ecology: This species always remains largely buried in sand or sediment in depths of up to 80 m; its base is attached to substrates like rock, stone or shell, with only the oral disc and tentacles visible. Biology Description: Column is translucent white with white spots, and it grows to approximately 7 cm in diameter. Oral disc may reach 12 cm and overall diameter with the tentacles spread out is about 30 cm. This species usually has ﬁve whorls of tentacles, with 96 tentacles. Tentacles are each around 8 cm long, green to yellow in colour, and sometimes greyish. They often have bands of white and other colours, and purple tips. Mouth, in the centre of the oral disc, is purplish. Life cycle: This sea anemone reproduces in spring and summer by releasing gametes into the water column where they are fertilized and develop into planula 6.2 Family Actiniidae 199 larvae. Alternatively, the gametes can be retained in the body cavity and the larvae are brooded there till the spring. Association: The shrimp species Periclimenes aegylios may be found living symbiotically with this sea anemone. Envenomation: Anderluh and Macek (2012) reported on the presence of cytolytic peptide and protein toxins (cytolysins) in the venom of this species. Rosenberg (1978) reported on the presence of four neurotoxins in this species.

Condylactis gigantea Weinland, 1860 (¼ Condylactis passiﬂora)

Image credit: Nhobgood Nick Hobgood; Wikipedia Common name (s): Condylactis anemone, giant golden anemone, giant Carib- bean Sea anemone Global distribution: Caribbean Sea more specifically the West Indies; and western Atlantic Ocean including southern Florida through the Florida Keys. Ecology: It is found in shallow reefs and other shallow inshore areas; in the crevices of rock walls; attached to a rock, shell or almost any other hard objects; and is very common around reefs in both “forereef” and lagoon areas. It can also be found at most inshore areas, on coral reefs, though this is less common. Biology Description: It is approximately 15 cm high and 30 cm wide, making the disc diameter approximately 40 cm. It is a large, columnar animal and can exhibit a variety of colours: white, light blue, pink, orange, pale red or light brown. Its mouth is surrounded by 100 or more tentacles which differ in each individual of the species and their tips may be purple or rose coloured or they even may not have any change in colour, becoming paler than the body itself. Whole tentacles are shades of either brown or greenish and its basal disc is firmly attached to the substrate with the only “free–floating” portion, i.e. tentacles. 200 6 Biology and Ecology of the Venomous Marine Anthozoans (Class Anthozoa)

Food and feeding: It is a macrophagous carnivore and feeds upon fish, mussels, shrimp, zooplankton and sea worms. Predators: Its predators are red leg hermits, grey sea slug or the tompot blenny. Life cycle: This anemone is generally dioecious, but it is occasionally hermaphro ditic. It has a 1:1 sex ratio (males to females); there is no evidence of brooding or of asexual reproduction or division furrowing. Its reproduction scheme has been defined as oviparous ! planktonic ! lecithotrophic. The releasing or spawning of eggs and sperm is relatively synchronous with fertilization occurring externally in the water column. Fertilized egg produces a planula larva. The planula larva will settle on the benthos, develop a pedal disc, and then eventually grow into a fully developed anemone. Association: This species plays an important role in their subtidal communities by providing shelter to a variety of commensals (several fish and cleaner shrimp species), and they serve as “base stations” for fish cleaning activity. Envenomation: The CgNa toxin present in the nematocysts of this species when discharged causes extreme pain and paralysis (Anon. https://en.wikipedia.org/wiki/ Condylactis_gigantea). Shiomi et al. (1997) reported on the presence of sodium channel toxin in this species. Frazão et al. (2012) reported on the presence of NaV channel toxins CgNa and Cp I and PLA2 toxins like phospholipase A2 in this species. Yost and O’Brien (1978) reported on the isolation of two components of its toxin and their LD50 values of 19 and 58 μg/kg, respectively, when injected into Armadillidium vulgare, a terrestrial crustacean. Ständker et al. (2006) reported on the presence of a new peptide, sodium channel toxin (CgNa), with strong paralytic activity; sodium channel inactivation and cardiac excitation–contraction coupling.

Doﬂeinia armata Wassilieff, 1908 6.2 Family Actiniidae 201

Image credit: Mutsu-sango, Wikipedia Common name (s): Striped anemone, armed anemone, glass sea anemone Global distribution: Tropical waters of Australia as far south as Perth and Western Australia; Philippines and Indonesia. Ecology: This species which is found in fine silt or mud lives at depths of up to 20 m in the intertidal zone on sloping, sheltered reefs, as well as in mangroves. Biology Description: It is one of Australia’s largest species of anemone and it can grow to 20 cm in diameter, with tentacles up to 50 cm long. Base of this species is broad; and column is smooth, with a broad, flat oral disc. It has long inner tentacles which are a minimum of double the size of the outer tentacles. Surface of the tentacles end in a tip that is somewhat swollen. These tentacles are either cream, brown or plain, and are striped. They have a surface that is scale-like and are often observed curling into ball shapes that hide the mouth. Tentacles have visible papillae on the surface. Papillae of its oral disc also contain nematocysts. This anemone is able to expand its body and tentacles due to a well-developed hydrostatic system. Envenomation: Sting of this most toxic sea anemone presents a danger to humans. Injuries resulting from contact with this species are considered very painful and can take several months to heal (Anon. https://en.wikipedia.org/wiki/Dofleinia_ armata, http://www.globetrotterscience.com/uploads/2/1/8/4/21849914/ms_chap ter_8.pdf). Anon. (https://www.uniprot.org/uniprot/P0DMZ2) reported on the presence of a delta-actitoxin-Dar1b which binds specifically to voltage-gated sodium channels (Nav), thereby delaying their inactivation during signal transduction.

Entacmaea quadricolor (Leuckart in Rüppell & Leuckart, 1828) (¼ Physobrachia douglasi; Gyrostoma helianthus; Parasicyonis actinostoloides) 202 6 Biology and Ecology of the Venomous Marine Anthozoans (Class Anthozoa)

Image credit: Nhobgood Nick Hobgood, Wikipedia Common name (s): Bubble-tip anemone Global distribution: Widespread throughout the tropical waters of the Indo- Pacific area, including the Red Sea. Ecology: It has a planktonic habitat. Biology Description: These anemones which grow up to a diameter of 40 cm appear in a variety of morphs, including rose, orange, red and standard green. Its tentacles are 4–6 cm long and they may have bulbous tips. There may be a white “equator” around the bulbous portion. When not inflated, tip is then blunt with a white ring where the “equator” would be. This bulbous tip seems to be related to the presence of anemonefish and can disappear. Body column is smooth with no verrucae. It has a small pedal disc. Food and feeding: It obtains most of its energy from solar radiation via its symbiotic zooxanthellae. Predators: Life cycle: It reproduces asexually or sexually. Association: A characteristic of this species is its ability to maintain a symbiotic relationship with the anemonefish, which can be “hosted” by the anemone by providing it with defence against predators and also providing some nourishment. In turn, the anemone provides the anemonefish with shelter. Envenomation: Like other sea anemones, this venomous anemone has stingers in its tentacles that can inflict a painful sting (Blaxter et al. 1984; Anon. http://www. wildsingapore.com/wildfacts/cnidaria/actiniaria/entacmaea.htm). Anon. (https://www.uniprot.org/uniprot/Q8ISF8) reported on the presence of a toxin, red fluorescent protein eqFP611, from this species. delta-actitoxin-Eqd1a (Anon. https://www.uniprot.org/uniprot/P09949) reported on the presence of a toxin, delta-actitoxin-Eqd1a, from this species. Anderluh and Macek (2012) reported on the presence of cytolytic peptide and protein toxins (cytolysins) from this species. Marsh and Slack-Smith (2010) reported that this species contains toxins which can break down the cell membranes and can be deadly if eaten. Further more than 40 toxic peptides have been isolated from this species.

Epiactis japonica (Verrill, 1869) (¼ Cnidopus japonicus; Aulactinia japonicus) 6.2 Family Actiniidae 203

Common name (s): Sea anemone Global distribution: North-west Pacific: from Aleutian Islands to Kamchatka and to Japan. Ecology: It always lives on exposed surfaces of stones or rock; newer buried in sand; and never attach gravel or other particles to itself. Biology Description: Body of this species may be smooth or with non-adhesive tubercles. Colouration is extremely variable: red, yellow, green, etc. There are numerous crowded, often rectangular vesicles arranged in several rows on the lowest portion of column and are containing extremely numerous nematocysts (striking capsules) of a special sort. Some specimens of this species may have special fighting tentacles (also called catch tentacles). Fighting tentacles are longer than the typical tentacles; and they are often coiled, but the main feature of fighting tentacles is special set of nematocysts. It contains chromo protein and is a bioluminescent species (Corals. https://www.reeflex.net/tiere/8907_Epiactis_japonica.htm). Envenomation: Its toxin, AnmTx Cj 1c-1, has been reported to induce marked paralysis on shrimps at 10–20 s after injection and a weak toxicity when injected into fly larvae (Anon. https://www.uniprot.org/uniprot/P0DPE5). Babenko et al. (2017) reported that the toxin of this species has neurotoxins, toxin-like molecules, linear polypeptides (Cys-free), enzymes and cytolytics. Anderluh and Macek (2012) reported on the presence of cytolytic peptide and protein toxins (cytolysins) from this species.

Epiactis prolifera Verrill,1869

Common name (s): Brooding, proliferating or small green anemone Global distribution: North-eastern Paciﬁc. Ecology: It lives in highest density on or under rocks in the sublittoral zone, in surge channels, on rock shelves and areas exposed to wave action. It is often found in areas encrusted with coralline algae and sometimes grows on the leaves of eelgrass. 204 6 Biology and Ecology of the Venomous Marine Anthozoans (Class Anthozoa)

Biology Description: This species grows up to 3 cm in height and up to 5 cm in diameter and varies in colour. It is greenish brown but sometimes brown, pink, red or dull green. There are fine white lines starting at the mouth and spreading radially across the oral disc and further white lines occur on the column and pedal disc. Lower part of the column and pedal disc are occasionally blue. There are often radiating pale and dark lines on the edges of the pedal disc and the lower part of the column. Mouth is surrounded by 48 to 96 short, conical tentacles, and each of them is tipped with a terminal pore. Food and feeding: The diet of this species consists of small fish, shrimps, crabs and jellyfish. During feeding, the prey is immobilized by the nematocysts present in the tentacles which inject toxins, then passed by the tentacles through the mouth and into the gastrovascular cavity. Any undigested wastes are expelled through the mouth. Predators: Predators of this specie include the nudibranch Aeolidia papillosa, the leather star Dermasterias imbricata and certain fish. Life cycle: It is a protogynic hermaphrodite. The young start life as females, but when the pedal disc is about 2 cm in diameter, they develop testes on the mesentery and spend the rest of their life as hermaphrodites. This means that the population consists of a large number of young females and a small number of older hermaphrodites. Sperm is released into the water column and after cross-fertilization (or sometimes self-fertilization), the young remain within the mother’s gastrovascular cavity during their early development. The mother then sends out a mass of eggs and mucus through her mouth and they spread across her oral disc. Cilia move some of them down the column and they become attached to the base of the column with mucus. The larvae develop tentacles of their own and grow in a protective environment for about 3 months. When they reach about 4 mm in diameter, they separate from their mother and move away to live independently. Association: This anemone sometimes displays mutualism by attaching itself to a hermit crab or decorator crab. The anemone provides protection for the host from predators and it is benefitted by consuming the food fragments discarded by the crab. Further, the copepod, Doridicola sunnivae,isanectoparasite of the brooding anemone. Envenomation: Anderluh and Macek (2012) reported that the venom of this species contains cytolytic peptide and protein toxins (cytolysins). 6.2 Family Actiniidae 205

Isactinia citrina (Haddon & Shackleton, 1893) (¼ Telactinia citrina)

No information is available on the Biology and Ecology of this species. Envenomation: The peptide toxin of this species has been reported to block K+ (potassium) channels. Changes in K+ channel function have been associated with cardiac hypertrophy and failure, apoptosis and oncogenesis, and various neurodegenerative and neuromuscular disorders (Yamaguchi et al. 2010).

Macrodactyla doreensis (Quoy & Gaimard, 1833)

Image courtesy: cs:ŠJů, Wikipedia Common name (s): Corkscrew tentacle sea anemone, snaky anemone Global distribution: Japan, New Guinea and northern Australia. 206 6 Biology and Ecology of the Venomous Marine Anthozoans (Class Anthozoa)

Ecology: This species is commonly found on coral rubble and near seagrasses and reefs at depths of 5 m or less in muddy bottoms; remains at the surface of the sediment, with the column buried; and is commonly seen where there is no fish population. Biology Description: It has a flared/corkscrew shape, and grows to a maximum of 5 cm wide, but is often far smaller. It has white lines that are oriented radially, sometimes extending onto the tentacles which are snaky, thick and long (about 10 cm). These tentacles may be brown, green or purplish, but tips may be darker or lighter; and they are tightly coiled or curled especially when the sea anemone is submerged. Lower portion of the column is a dull orange to bright red colour and upper portion is brownish, containing a round to ovoid verrucae in rows oriented longitudinally. This anemone harbours symbiotic algae, zooxanthellae that photosynthesize and share the food produced with the anemone, which in turn provides the algae with shelter and minerals. Association: Several kinds of animals have been found associated with snaky anemones including anemone shrimps (Periclimenes sp.) and anemonefishes (Amphiprion spp.) including A. biaculeatus, A. clarkii (juvenile and adult), A. percula, A. perideraion and A. polymnus (juvenile and adult). But these are rarely observed on these anemones during low tide. Envenomation: The peptide toxin of this species has been reported to block K+ (potassium) channels (Yamaguchi et al. 2010). Further, the venom of this species exhibited weak haemolytic activity against ovine erythrocytes (Nedosyko et al. 2014).

Mesactinia ganensis England, 1987

No information is available on the Biology and Ecology of this species. Envenomation: The peptide toxin of this species has been reported to block K+ (potassium) channels (Yamaguchi et al. 2010). 6.2 Family Actiniidae 207

Oulactis orientalis (Averincev, 1967)

Common name (s): None Global distribution: Peter the Great Bay (Amur Bay, Sea of Japan), Kurile Islands (Russia). Ecology: It is found in the intertidal zone up to a depth of 4–5 m, where it attaches by a pedal disk to small boulders and pebbles covered with thin layer of sand; and it is submerged leaving outside only its oral disk with tentacles. Biology Description: Column of this species is cylindrical. It grows up to 80 mm height and 50 mm in diameter and is divided into scapus and capitulum with a parapet and fosse. Pedal disc equals in diameter to column. Scapus bears adhesive verrucae which are arranged in longitudinal rows and are bearing shells, gravel and sand. In the upper part of the column, verrucae are divided into lobes. Acrorhagi are present in parapet’s region. Column is yellow-grey or grey colour; and tentacles are green, yellow, brown or wine-, olive-coloured, with white transversal strips. Sphincter is strong and circumscribed. Actinopharynx is with two siphonoglyphs. Tentacles which are up to 72 in number are of moderate length and tapering. Mesenteries are arranged hexamerously in three to ﬁve cycles. Food and feeding: This species is omnivorous with a certain shift towards zoopolyphagy. During the process of feeding, it demonstrates no selective behaviour and uses only the existing food reserves. Life cycle: It is dioecious with cross fertilization. Further details in this aspect are wanting. Envenomation: Two cytolytic toxins (cytolysins) Actinoporin Or-A and Actinoporin Or-G which possess haemolytic activities have been isolated from this species (Il’ina et al. 2005; Frazão et al. 2012). 208 6 Biology and Ecology of the Venomous Marine Anthozoans (Class Anthozoa)

Paracondylactis sinensis Carlgren, 1934

Common name (s): Pearly sea anemone Global distribution: This species is endemic to Indian coast. Ecology: It dwells in intertidal sand and sandy mud area. Biology Description: This species has grey pigmented body, with smooth surface. It has long, thick tapering 96 tentacles arranged in five cycles. It is, however, difficult to observe all 96 tentacles because half of tentacles, coming out from near the mouth, are covering the other half of the tentacles. These tentacles are translucent, usually unpatterned and beige or pinkish. Oral disk is also usually unpatterned and sometimes slightly darker than the tentacles. Body column which is elongated and tapering is smooth and plain without any bumps. Pedal disc is flattened and distinct. Colour of the tentacles and oral disc is white to colourless. This species has the tendency to spread its tentacles outward, stretching its body size up to about 30 cm. As it covers its body underground, and is only exposing its tentacles, bottom half of the body is relatively thinner than upper half of the body. Envenomation: Yamaguchi et al. (2010) reported on the presence of a potassium channel toxin, κ1.3-SHTX-Hm1a (HmK), from this species. Anderluh and Macek (2012) reported on the presence of cytolytic peptide and protein toxins (cytolysins) with haemolytic activity from this species. Nedosyko et al. (2014) reported that the crude venom of this species showed erythrocyte haemolysis, artemia lethality and shore crab neurotoxicity. Ravindran et al. (2010) reported that the crude and partially purified venom of this species was cardiotoxic, nephrotoxic, hepatotoxic and neurotoxic to the internal organs of the mice. The associated chronic and lethal histopathological changes like haemolysis, thrombosis and myocardial haemorrhage in the heart; granulomatous lesions and damage to the hepatic cells in the liver and haemorrhage throughout the kidney parenchyma and shrinkage of granular tufts in the kidney. 6.2 Family Actiniidae 209

Phlyctenactis tuberculosa (Quoy & Gaimard, 1833)

Image credit: Wikimedia Commons Common name (s): Swimming anemone, wandering sea anemone Global distribution: Western Australia, Victoria, New South Wales, Tasmania and New Zealand. Ecology: This is a nocturnal, shallow water species, living in moderately exposed areas and among sheltered reefs at depths to 35 m. It attaches to rock, seagrasses and kelp, but it is also able to detach its pedal disc and is commonly found drifting on the sea ﬂoor. It moves about on the seabed by creeping with its basal disc, and at night climbs seagrasses or algae for the purpose of feeding. Biology Description: This is a large anemone and its body wall is covered with bubble-like sacks, and comes in a variety of colours from brownish orange, mauve, light grey to brown in colour. Tentacles are lighter and may be pale yellow, grey, brown or orange-yellow in colour. It grows to a maximum size of 15 cm in diameter with a column that can reach 25 cm long. During the day, it remains bundled together, appearing like a ball of baked beans. Envenomation: It is venomous and touching the tentacles can cause a painful sting (Marsh and Slack-Smith 2010; Anon. https://en.wikipedia.org/wiki/ Phlyctenactis_tuberculosa). 210 6 Biology and Ecology of the Venomous Marine Anthozoans (Class Anthozoa)

Phymactis clematis (Drayton in Dana,1846)

Image credit: Flickr Common name (s): Not designated Global distribution: Buenos Aires, Argentina. Ecology: it is found throughout the entire intertidal zone, from the midlittoral ﬂoor up to the infralittoral; it positions itself on hard substrates in open and unprotected zones as well as in crevices, tide pools and protected zones. Biology Description: Not reported. Association: The crab Allopetrolisthes spinifrons (Porcellanidae) has found to be symbiotic with this anemone. Envenomation: Anderluh and Macek (2012) reported that the cytolytic peptide and protein toxins (cytolysins) isolated from the nematocyst venom of this species possess haemolytic activity. The toxin, coelenterolysin (a single peptide or a group of peptides), isolated from this species has been found to possess haemolytic activity (Meinardi et al. 1994). 6.2 Family Actiniidae 211

Pseudactinia infecunda (McMurrich, 1893) (¼ Pseudactinia ﬂagellifera)

Common name (s): Red false plum anemone Global distribution: Indian Ocean: Mozambique, South Africa. Ecology: It is found singly or in small family groups in pools and shallow reefs up to 20 m. Biology Description: It is a large and conspicuous anemone. Column is smooth and cannot readily retract tentacles or close up. There are three to ﬁve rows of bubble-like vesicles and one row of spicules just outside the tentacles. Overall colour of the anemone is red with white lines on the tentacles. Mouth area can be white or greenish. Size of the animal is 50–100 mm in diameter. Life cycle: Reproduction can be sexual or by simple division of the body. Envenomation: Anderluh and Macek (2012) reported that the cytolytic peptide and protein toxins (cytolysins) isolated from the nematocyst venom of this species possess haemolytic activity. The most potent venom of this species has been reported to have a serious sting which is dangerous to humans (Anon. https://nl.wikipedia.org/wiki/Pseudactinia_ infecunda, https://sites.google.com/site/ecanemone/actiniidae/pseudactinia-ﬂagellifera- 1-red-false-plum-anemone). 212 6 Biology and Ecology of the Venomous Marine Anthozoans (Class Anthozoa)

Pseudactinia varia Carlgren, 1938

Common name (s): Mauve false plum anemone Global distribution: South Atlantic; South Africa. Ecology: This species is found in the intertidal zone; and infralittoral to 102 m. Biology Description: Column and tentacles of this species are rose red to red brown; tentacles are with white band at the base, some with violet tips; oral disc is grey; and marginal spherules and vesicles may be red. Oral disc diameter is 80 Â 70 mm, but most animals are smaller. There are 72 to >300 tentacles Häussermann and Försterra (2001). One to two rows of vesicles are seen on the distal region of the column. Sphincter muscle is diffuse and is strongly branched. There are up to 36 complete mesenteries. Food and feeding: It feeds on clams, crustaceans and snails. Life cycle: In this species, there is no asexual reproduction and longitudinal ﬁssion. Envenomation: Anderluh and Macek (2012) reported that the cytolytic peptide and protein toxins (cytolysins) of the nematocyst venom of this species possess haemolytic activity. Bernheimer et al. (1984) reported that the toxin termed variolysin (a protein) of this species possesses haemolytic activity. 6.2 Family Actiniidae 213

Urticina crassicornis Muellaer, 1776 (¼ Tealia crassicornis)

Common name (s): Mottled anemone, painted anemone, Christmas anemone Global distribution: North-eastern Pacific Ocean, North Atlantic Ocean, Arctic Ocean. Ecology: This benthic and sessile organism is commonly found in the lower intertidal and upper subtidal zones up to 30 m deep; and it is inhabiting well- protected and shaded areas on docks, wood pilings, and under large rock outcrop- ping and is firmly attached only to hard substrata. Biology Description: This is a biradially symmetrical species with a height of 2–12.7 cm and a width of 1–7.6 cm. It has a solid basal plate which is always flat. Its column is olive green with or without red spots; solid red; cream or brown, always with small, inconspicuous tubercles but without acontia. Its tubercles are not white and do not usually accumulate bits of sand, gravel and shell. Its tentacles which are superior of the column are usually 100 in number and are green to opaque cream with red and white striations and semi-transparent when extended. These tentacles are conical, thick and blunt and are arranged in three to five circular rings around the oral disc. Oral disc has no white striations and it usually has the same colour scheme as the tentacles. Food and feeding: It is a non-selective and opportunistic predator feeding on crabs, sea urchins, mussels, gastropods, chitons, barnacles, fish and sometimes sea stars and stranded jellies. Its peculiar prey is the sun flower star, Pycnopodia helianthoides. This anemone exhibits both intracellular and extracellular digestion. Food is caught within the tentacles which then move the prey towards the oral disc. Predators: Certain species of both Asteroidea and Gastropoda are the known predators of this anemone. Demasterias imbricata (Asteroidea) and Aeolidia papillosa (Gastropoda) are two notably frequent predators of this species. 214 6 Biology and Ecology of the Venomous Marine Anthozoans (Class Anthozoa)

Life cycle: It has both asexual and sexual reproduction. In the Atlantic populations, eggs and sperm are fertilized within the body column. The young are brooded between the mesenteries of the body and are sent out as well-developed, young anemones. Spawning occurs in the spring amongst Puget Sound populations, when eggs and sperm are released into the sea for fertilization. After fertilization, a solid and ciliated blastula is formed and 6 days following fertilization, a cone-shaped and benthic, larval planula develops. These planulae then settle onto small rocks or the empty tubes of some annelid worms and develop into small anemones. After 12 days of settlement, eight tentacles appear. Further growth, however, is slow as 2 months after settlement, 12 tentacles appear and the anemone is only 0.88 mm in diameter; 1 year after settlement, the anemone has 35 tentacles and is 10 mm in diameter. This species is sexually mature with a diameter of 10–15 mm when it is about 1 year old. Envenomation: Frazão et al. (2012) reported on the presence of the toxin cytolysin Uc-I and PLA2 toxins UcPLA2 in this species. Anon. (https://www.uniprot.org/uniprot/C9EIC7) reported on the presence of DELTA-actitoxin, Ucs1a in this species and this toxin possesses haemolytic activity.

Urticina eques (Gosse, 1858) (¼ Urticina lofotensis; Tealia lofotensis)

Image credit: Jim Greenfield Common name (s): White-spotted rose anemone, strawberry anemone, horseman anemone Global distribution: North Atlantic Ocean and the Pacific coast of North America; northern Europe and entire coast of Norway. Ecology: It is found on rocks and pilings, in crevices and gullies and favours exposed habitats with fast-moving water. On soft substrata, it is frequently found attached to the inside of an empty bivalve shell (Pecten, Arctica, etc.) and are lying loose on the bottom. Its depth range is from below the intertidal zone and down to 400 m. Biology Description: Base of this species is not much wider than the column and is firmly adherent. Column is equal in height and diameter or a little taller, with a prominent parapet and deep fosse; and is slightly softer in texture. Verrucae are numerous but 6.2 Family Actiniidae 215 unobtrusive and are often not raised above the surface of the scapus. They are non-adhesive and are never having gravel stuck to them. Tentacles which are up to 200 are stout and moderate in length; and are arranged in five to six cycles. Body is usually brighter and more translucent. Column is dirty white, pink, yellowish, red or orange, and the paler forms are usually blotched with red or orange. Verrucae are forming whitish spots which may be obscure on the pale varieties. Disc and tentacles are similar to column and are rarely grey, brown or magenta. Oral disc is with a pattern of red lines and tentacles are fairly translucent, banded or plain. Its base diameter is up to 20 cm and span of tentacles is up to 30 cm. Life cycle: It is dioecious. In California, female ripeness occurs in December as the sea temperature begins to fall. The large eggs are produced at intervals, and the release of sperm by the males follows shortly afterwards. In some females, large oocytes also release eggs at other times of year. The gametes emerge through the mouth of the anemone and fertilization is external. The eggs develop into planula larvae which drift with the current before settling and growing into juveniles. Association: Juveniles of the painted greenling, Oxylebius pictus a species of marine fish, have a facultative association with this species. They are often found among the tentacles or close to the column, especially when resting and inactive at night. Envenomation: Anderluh and Macek (2012) reported that the nematocyst venom of this species contains cytolytic peptide and protein toxins (cytolysins) with haemolytic activity. Logashina et al. (2017) reported on the presence of a toxin (peptide) τ-AnmTx Ueq 12-1 (short name Ueq 12-1) in this species.

Urticina felina (Linnaeus, 1761) (¼ Tealia felina) 216 6 Biology and Ecology of the Venomous Marine Anthozoans (Class Anthozoa)

Common name (s): Dahlia anemone Global distribution: Arctic Ocean, Baltic Sea, North Sea and northern Atlantic Ocean; Bay of Biscay and Gulf of Maine. Ecology: It is found attached to rock on the sea bed and other organisms; occurs in rock pools, in crevices and gullies; and among the holdfasts of Laminaria spp., in caves and partly buried in gravel from the lower tidal limit down to a depth of 100 m. Biology Description: Base of this species is up to 120 mm across. Deep sea specimens are usually larger than inshore ones. Column is usually shorter than its diameter and its surface is covered in verrucae. There is a parapet at the top where the verrucae are organized into rows. These verrucae usually have bits of gravel and debris attached to them and the contracted anemone has the appearance of a rounded hummock of gravel. Oral disc is not broader than the parapet and it has up to 160 short tentacles arranged in multiples of ten. Its colour is variable, from deep red to brown or purplish, with green spots and darker tentacles. Tentacles are stout, short and are often banded; and in many individuals there are thin red lines on the disc visible between the tentacles. Food and feeding: Its diet comprises small ﬁsh and crustaceans, which they immobilize by ﬁring groups of stinging cells (cnidae) into them. Envenomation: Anderluh and Macek (2012) reported on the presence of cytolytic peptide and protein toxins (cytolysins) in the nematocyst venom of this species. These toxins possess haemolytic activity.

Urticina lofotensis (Danielssen, 1890)(¼ Tealia (Utricina) lofotensis)

Image credit: Wikimedia Commons Common name (s): White-spotted anemone, white-spotted rose anemone, strawberry anemone Global distribution: SE Alaska to San Diego, CA; North Atlantic. 6.2 Family Actiniidae 217

Ecology: It is mostly low intertidal (subtidal) to 15 m. It is rocky and is found on exposed coast, concrete pilings and marina ﬂoats. Biology Description: This large anemone has no acontia. Column is red with smooth white tubercles in longitudinal rows. Margin of the oral disk has no white spherules. Tubercles usually do not hold sand, shells or other debris. Oral disk is red and has no radiating white stripes. Its slender tentacles are red, unbanded but with sometimes a yellow tinge at the base and pinker at the tips. Diameter of the anemone is up to 10 cm. Life cycle: The eggs are very large (over 1.2 mm diameter) and yolky. It has not been observed brooding the eggs. Association: Juvenile painted greenlings (scorpaenoid ﬁsh) are often associated with this anemone, and adults may sleep near its base. Envenomation: Anderluh and Macek (2012) reported on the presence of cytolytic peptide and protein toxins (cytolysins) with haemolytic activity in this species.

Urticina piscivora (Sebens & Laakso, 1978)

Image credit: Wikimedia Commons Common name (s): Fish-eating anemone, fish-eating urticina Global distribution: North-east Pacific: from Alaska in the north, down to La Jolla, California, in the south. Ecology: It most commonly inhabits exposed, rocky subtidal areas of the coastlines. It attaches itself to rocky prominences in locations with a substantial current flowing past. Biology Description: It is a large anemone, growing to a maximum height of about 20 cm and a diameter of about 10 cm. Column is bright red in colour. Acontia is absent, but 218 6 Biology and Ecology of the Venomous Marine Anthozoans (Class Anthozoa) it has tubercles. These are not white and are arranged in circumferential rows. Normally they do not accumulate debris such as shells and sand. This anemone is made up of three layers of cells called the epidermis, the mesoglea and the gastrodermis or gastrovascular cavity which functions as the gut of the anemone. Gut is divided into compartments by sheets of tissue called “septa”. These sheets of tissue develop into tentacles on the surface of the anemone. Tentacles are found in multiples of six. Food and feeding: As its name suggests, this species is capable of capturing and consuming small fishes and shrimp. It does so through the use of its tentacles, stinging its prey with a potent toxin which paralyses them. Life cycle: This anemone is dioecious, meaning that it has distinct male and female individual organisms. They reproduce sexually through the external fertilization of egg and sperm. The produced larvae will float in the current until they eventually land. Afterwards the larvae will attach to the bottom and develop a pedal disk which will grow as juvenile anemones. Association: Oxylebius pictus (the painted greenling) and Lebbeus grandimanus (candy stripe shrimp) have the ability to remain among the tentacles of this species without being harmed. Envenomation: Their sting of this species can be severely painful for humans (Anon. https://en.wikipedia.org/wiki/Urticina_piscivora). Cline et al. (1995), Frazão et al. (2012) and Anderluh and Macek (2012) reported on the presence of a potent cardiac stimulatory protein (cytolysin), Up-1, in the tentacle toxin of this species. Further, the extract of this species was found to be a potent haemolysin on erythrocytes of rat, guinea pig, dog, pig and human, causing haemolysis.

6.3 Family Actinodendridae

Actinodendron alcyonoideum (Quoy & Gaimard, 1833) Image not available Common name (s): Not designated Global distribution: Tropical eastern central Paciﬁc, eastern Indian Ocean, western central Paciﬁc. Ecology: It is found on soft sediment, usually sand. Biology Description: Not reported. Envenomation: The very potent toxin present in its tentacles has been known to sting divers quite badly (Anon. http://animal-world.com/Aquarium-Coral-Reefs/ Hells-Fire-Anemone). 6.3 Family Actinodendridae 219

Actinodendron arboreum (Quoy & Gaimard, 1833)

Image credit: Wikimedia Commons Common name (s): Tree anemone, hell’s fire anemone Global distribution: Tropical eastern Indian Ocean and western Pacific. Ecology: This sessile species is found at depths of down to 28 m. Biology Description: In this species, its oral is only seen as the pillar-like column is burrowed into the soft sediment. There are 48 tentacles which are completely branched so as to resemble the head of broccoli. Tentacles, oral disc and column are sand-coloured. Oral disc may have radiating white lines; column is smooth with many small dark splotches, some with crimson spots near base. Oral disc diameter is about the same length as extended tentacles that is about 100 mm and column may be 120 mm long. Food and feeding: This anemone is a carnivore and will generally accept meaty foods like shrimp, krill and mussels. Predators: It is unknown if this species has any predators. Life cycle: It can multiply by sexual and asexual means. By sexual reproduction, ciliated planula larvae result. This planula will eventually fall to the sea floor, develop a pedal disk, then begin to grow into a new juvenile anemone. Envenomation: These anemones have a very potent toxin in their tentacles and they have been known to sting divers quite badly (Anon. http://animal-world.com/ Aquarium-Coral-Reefs/Hells-Fire-Anemone). It is highly venomous and its sting can cause severe skin ulcers (as also suggested by its alternative name, hell’s fire anemone) (Anon. https://en.wikipedia.org/wiki/ Actinodendron_arboreum).

Actinodendron glomeratum Haddon, 1898 Image not available Common name (s): Branching anemone Global distribution: Tropical western central Paciﬁc; entire Indo-Paciﬁc region. 220 6 Biology and Ecology of the Venomous Marine Anthozoans (Class Anthozoa)

Ecology: It can be found on sandy bottoms in a depth range of 0–5m. Biology Description: It is a large anemone with robust tentacles, covered in clusters of vesicles. It is green colour at the mouth, and is with numerous dark dots, running up the branches. When touched, it can expel water and retract into the bottom very quickly. Its size is up to 30 cm in diameter. Food and feeding: It feeds on plankton. Its symbiotic zooxanthellae also help in its nutrition. Association: These anemones have symbiotic relationship with shrimps belonging to the genus Periclimenes. Envenomation: These anemones have a very potent toxin in their tentacles and they have been known to sting divers quite badly (Anon. http://animal-world.com/ Aquarium-Coral-Reefs/Hells-Fire-Anemone). Anon. (https://www.peerintoyourworld.com/species/actinodendronidae/ actinodendron-glomeratum-branching-anemone/) reported that this anemone can deliver a painful and powerful sting.

Actinodendron hansingorum Carlgren, 1900 Image not available No information is available about the Biology and Ecology of this species. Envenomation: These anemone have a very potent toxin in their tentacles and they have been known to sting divers quite badly (Anon. http://animal-world.com/ Aquarium-Coral-Reefs/Hells-Fire-Anemone).

Actinodendron plumosum Haddon, 1898

Common name (s): Hell’s fire sea Anemone, branching anemone Global distribution: Tropical waters of the Indo-Pacific; western central Pacific: New Caledonia and Palau; Great Barrier Reef. 6.4 Family Agariciidae 221

Ecology: It is a burrowing anemone seen in sand ﬂats, lagoon sand and Halimeda patches. It buries its foot and body in the sand with only its oral disc and tentacles are emerging. When disturbed, it can retract its entire body into the sand and it will be virtually invisible. This anemone comes out at night and hides during the day. Biology Description: It is a solitary anemone attaining a diameter of 30 cm. Colour of these anemones can be light yellowish green, tan, brown, light green or grey. Each of its tentacles varies in size and has more of a “frilly” look to it. From a distance it almost looks like soft coral, like a kenya tree. Association: These anemones are often occupied by commensal shrimp Ancylocaris brevicarpalis and Ancylomenes tosaensis. Envenomation: These anemones have a very potent toxin in their tentacles and they have been known to sting divers quite badly (Anon. http://animal-world.com/ Aquarium-Coral-Reefs/Hells-Fire-Anemone). Prentis et al. (2018) reported that most injuries caused by these anemones are associated with skin rashes and oedema.

Actinodendron sp. Envenomation: Jouiaei (2016) reported that this unidentiﬁed hell’s ﬁre anemone contains PLA2 toxins which are responsible for human envenomation. Further, its toxin α3β2 has been reported to be nAChR blocker.

6.4 Family Agariciidae

Pavona venosa (Ehrenberg, 1834) (¼ Pavona obtusata)

Common name (s): Foliose coral Global distribution: It is a common species on the Togian reefs of Indonesian coast. Ecology: It is a coral reef-associated species. Biology 222 6 Biology and Ecology of the Venomous Marine Anthozoans (Class Anthozoa)

Description: It is a massive colony with a diameter of 190 mm. Corallites are individually surrounded by a wall. In places and especially along the edge of the same colony, the calices may be arranged serially in small valleys. Association: Many small barnacles are found growing on its surface. Where these occur in a more or less linear arrangement close to each other, they hamper the growth of the corallites and cause a mammillated (covered with rounded protuberances) aspect of the surface. Envenomation: It is a venomous species (Blaxter et al. 1984) and its venomology is to be known.

6.5 Family Aiptasiidae

Aiptasia diaphana (Rapp, 1829)

Common name (s): Yellow aiptasia, glasrose Global distribution: Subtropical, Atlantic and Mediterranean: Canary Islands and Portugal; temperate eastern Atlantic Ocean; Red Sea. Ecology: This solitary, sessile and shallow water species is found on hard surfaces; it favours areas with poor water quality such as harbours and lagoons; depth range 2–25 m. Biology Description: It is a small sea anemone with a base diameter of up to 30 mm, a column height of up to 50 mm and an oral disc of 30 mm. Column is yellowish brown or brownish green, smooth and retractable. Colour is somewhat variable because symbiotic algae (zooxanthellae) are sometimes present in the tissues. Oral 6.5 Family Aiptasiidae 223 disc is transparent and bears, round the rim, four or five whorls of slender, pointed tentacles making a total of up to 160 tentacles. These are translucent with white bases, a distinguishing feature for this species. Food and feeding: It catches passing invertebrates, marine larvae and small fish with its tentacles, immobilizing the prey with its cnidocytes (stinging cells). It also obtains nourishment from its symbiotic zooxanthellae in its tissues. These photosynthetic algae manufacture carbohydrates in sunlight and these nutrients are made available to the sea anemone. Life cycle: It reproduces by both sexual and asexual reproduction under different conditions. In summer, the main method is pedal laceration where the sea anemone crawls along the substrate and fragments of the base become detached; and each fragment is growing into a new individual. Under laboratory conditions, an adult female can produce males, females and hermaphrodite individuals in this way. Envenomation: The solutes of this species released from these nematocysts through discharge contain five different protein components which exhibited haemolytic activity (Schlesinger et al. 2009).

Aiptasia mutabilis (Gravenhorst, 1831)

Common name (s): Trumpet anemone, rock anemone and glass anemone Global distribution: Subtropical; Cold waters of the Atlantic Ocean: from Ireland to the Canary Islands; Adriatic, Greek Aegean and Mediterranean Sea. Ecology: This benthic species is found on the lower shore in pools, and under stones or beneath overhangs, and are often seen amongst algal holdfasts, particularly 224 6 Biology and Ecology of the Venomous Marine Anthozoans (Class Anthozoa)

Laminaria and Saccorhiza. Sometimes it is abundant on infralittoral rock at wave sheltered locations. Its depth range is 0–50 m. Biology Description: It is a tall anemone, up to 12 cm high. Oral disc (tentacles not included) is 6 cm in diameter. Its slender column is flaring outwards to the broad oral disc. Tentacles which are about 100 and are laid out in 6 crowns around the siphonoglyph. They are steeply graduated in size; and inner ones are very long in extension, stout at the base and tapering to fine points. They are perfectly retractile but rarely retracted. Overall brownish colouration may have a blue tint. Column is brown and is often with irregular streaks of opaque white and tentacles are brown becoming paler and whitish towards their tips. Predators: Butterfly fish (Chaetodon kleinii, Chaetodon lunula, Chelmon rostratus, etc.), file fish (Acreichthys tomentosus), pufferfish (Canthigaster solandri, Arothron meleagris), nudibranchs (Aeolidiella stephanieae), some shrimp species (Lysmata wurdemanni, Rhynchocinetes durbanensis) and hermit crabs (Dardanus megistos). Life cycle: It has been known to reproduce both asexually and sexually. But asexual reproduction has been most commonly seen in this species. To reproduce asexually, the anemone splits the column and separates. These two separate parts will then adhere to a substrate, and individuals will begin to develop from these smaller amounts of tissue from the original individual. In sexual reproduction, zygote develops into a larva which settles and develops into its adult form. Association: This species acts as a host to many different organisms. Algae, rich in fucoxanthin, contribute to its dark brown colouring, and when these algae are not present, the organisms become a lighter, white colour. Other species involved in symbiotic relationships with this species are shrimp Periclimenes amestysteus and amphipod Caprella acanthiifera, which can be found in the tentacles of the organism, while the crabs Pilumnus spinifer and Eriphia verrucosa nest near the anemone and use it for protection. Dinoflagellates, particularly Symbiodinium sp., have also been known to have a symbiotic relationship with this species. Envenomation: Mariottini and Pane (2014) reported that the crude venom of this species showed response haemolytic effects against human erythrocytes. 6.5 Family Aiptasiidae 225

Exaiptasia diaphana (Rapp, 1829) (¼ Exaiptasia pallida; Aiptasia pallida)

Common name (s): Pale anemone Global distribution: North Carolina, Caribbean and Gulf of Mexico. Ecology: These small brown anemones are common in lagoon Halimeda patches and in some areas around rocks on shallow lagoon, mangrove roots and seaward reefs. They can be found thickly growing on buoy lines, particularly those that mark lagoon bottom shipwrecks. Biology Description: This anemone is transparent with brown, yellow or green colour provided by embedded photosynthetic cells called zooxanthellae. Pedal disc is up to 10 mm in diameter and is wider than column. Column is smooth and is up to 60 mm in height and 30 mm in diameter. Cinclides are often conspicuous in mid-column, in two to three rows, with ~12 cinclides per row. Mesenterial insertions are visible. Oral disc is 10 mm diameter. Tentacles (96) are smooth, long and are tapering towards tips. They are 20 mm in length. In living specimens, column is translucent proximally and greyish or brownish with scattered spots distally. Oral disc and tentacles are greyish. Mouth is whitish and actinopharynx is with yellowish circle around. Predators: A species of nudibranch in the genus Berghia is a predator on these anemones. Envenomation: Frazão et al. (2012) and Maček (1992) reported on the presence of phospholipase A in the venom of this species. This toxin is lethal for both invertebrates and vertebrates and is cardiotoxic, cutolytic and cytotoxic. Anderluh and Macek (2012) reported on the presence of cytolytic peptide and protein toxins in this species. Further they also reported on the PLA2 activity of the venom of this species. 226 6 Biology and Ecology of the Venomous Marine Anthozoans (Class Anthozoa)

6.6 Family Alcyoniidae

Sarcophyton glaucum (Quoy & Gaimard, 1833)

Common name (s): Rough leather coral, leather-soft mushroom Global distribution: Tropical to subtropical western Pacific: Red Sea, New Caledonia, Taiwan, Ryukyu Island and Palau. Ecology: It is found on the reef flats, in lagoons and on seaward slopes; it is very abundant and common in intertidal waters to considerable depths. It also inhabits soft bottom substrates, on muddy coastal areas to off-shore environments, and also in turbid near-shore reefs. Biology Description: This species grows up to 80 cm and it tends to be rather plain in colour. Its flesh is a yellow/tan and the polyps, which are rather long when extended, are typically tipped in green. Its capitulum is also less convoluted (folding). Envenomation: The main toxin sarcophine of this venomous species has been reported to be toxic to mice, rats and guinea pigs, and it showed strong anti- acetylcholine action on the isolated guinea pig ileum. Sarcophine was also a competitive inhibitor of cholinesterase in vitro (Ne’eman et al. 1975; Blaxter et al. 1984). 6.6 Family Alcyoniidae 227

Sarcophyton trocheliophorum von Marenzeller, 1886

Image credit: Gianemilio Rusconi Common name (s): Fleshy soft coral, elephant ear coral. Global distribution: Tropical to subtropical; Indo-Pacific. Ecology: It is a sessile species. Biology Description: This species develops many deep folds on its cap as it matures. It is a hardy species and has a ruffled appearance. Capitulum of this species is very convoluted (many deep folds), almost giving it a cauliflower appearance. Its extended polyps are shorter and finer and are brown or green. It also grows very large, up to 91 cm across and 91–122 cm tall. Body colour is yellow/tan, cream or tan. It is firm and soft and is easily torn. Envenomation: Mariottini and Pane (2014) reported that the toxin of this venomous species possesses haemolytic activity.

Sinularia abrupta Tixier Durivault, 1970 228 6 Biology and Ecology of the Venomous Marine Anthozoans (Class Anthozoa)

Common name (s): Smooth leathery soft coral, Okinawan soft coral Global distribution: Tropical western central Paciﬁc: Palau. Ecology: It is a benthic species. Biology Description: Colonies of this species have sterile stalks of 40–55 mm high. Its thick, ﬂattened lobes reach a length of about 50 mm, and thickness is 6 mm. Sometimes they are digitiform, but usually they are branched, or form twisted crests. Polyps are retracted within small pits. In the surface layer of the lobes, there are foliaceous clubs which are 0.08–0.20 mm long. In the outer layer of the sterile stalk, the leaf clubs are slightly longer and wider, and clubs with a length of 0.15–0.20 mm have more spiny heads. In the coenenchyme of lobes and sterile stalk, there are spindles which are up to 4 mm long. They have a slight median constriction and are densely covered with large coarse warts. Colour is yellowish light brown. Envenomation: It is a venomous species (Blaxter et al. 1984). Details of its toxicity, however, are not known.

6.7 Family Aliciidae

Alicia mirabilis Johnson, 1861

Image credit: Wikipedia Common name (s): Berried anemone, sea candles Global distribution: Indo-Paciﬁc: Azores, Portugal, Spain and the Mediterranean and Red Seas. 6.7 Family Aliciidae 229

Ecology: These phosphorescent sea anemones stand like pillar candles ﬁxed to the rocks, and both juveniles and adults have a nocturnal activity. Biology Description: Curled up during the day, this species resembles a brownish ball or dome covered with white, yellow or even brown protuberances. It unfolds at night and is in the form of a whitish translucent cylinder, carrying the same protuberances. Its column is up to 40 cm tall. Its tentacles when expanded may actually be longer than the column height. Both the tentacles and the “berries” contain stinging cells. It is bioluminescent. By day, these anemones look like ordinary sea anemone, but by night, they glow in the dark like delicate magical lanterns. Food and feeding: It is a passive carnivorous animal. Its tentacles which are equipped with stinging cells, the cnidoblasts, will strike the prey. The prey is brought to the mouth by the tentacles and digested inside the gastric cavity, divided by partitions. Each cubicle, between the partitions, corresponding to a tentacle. Life cycle: Reproduction occurs in this species mainly when external conditions are favourable, especially when the temperature of the water is temperate to warm. It is sexual and the individuals are separate sexes. Eggs and sperm are produced by the gonads located in the wall of internal septa. The fertilized eggs outside divide quickly to give after a few hours a swimming larva: the planula which gives rise to a polyp after falling on a suitable substrate. Further, there is also asexual reproduction by scissiparity where the animal will give an identical animal in every point: a clone. Envenomation: It is the most toxic sea anemone and can cause pain (Blaxter et al. 1984; Anon. http://www.globetrotterscience.com/uploads/2/1/8/4/21849914/ms_ chapter_8.pdf). Anon. (https://oceanexplorer.noaa.gov/explorations/03mex/logs/sept29/media/ 52.html) reported that this is a highly poisonous anemone, whose sting is toxic to all animals. 230 6 Biology and Ecology of the Venomous Marine Anthozoans (Class Anthozoa)

Lebrunia neglecta Duchassaing & Michelotti, 1860 (¼ Lebrunea danae)

Image credit: Fernando Herranz Martín, Wikipedia Common name (s): Not designated Global distribution: Bermuda, Bahamas, Caribbean Sea, Gulf of Mexico and north coast of Brazil. Ecology: It grows in reef environments at a depth of 2–60 m with its column hidden in a crevice in the rock or in a massive coral head. Biology Description: It is an unusual sea anemone in that its tentacles are almost hidden by the ring of six much branching large frond-like pseudotentacles that grow up from the rim of the oral disc. These tentacles of pale or darker brown and have densely branched tips. Below these, on the side of the frond are small, whitish spherical vesicles containing nematocysts. Column of the anemone is usually invisible and is anchored in a crevice. This species can grow to a diameter of 20 cm. Food and feeding: This is carnivorous species. After contact with a prey item, the pseudotentacles of this species retract and the tentacles, which are also armed with nematocysts, grasp the prey and draw it into the mouth. Association: The tissues of this specie contain the symbiotic unicellular alga Symbiodinium sp. This is photosynthetic and provides the anemone with energy. Further, a number of different invertebrates live in close association with this species. These include Pederson’s cleaning shrimp (Ancylomenes pedersoni), the spotted cleaner shrimp (Periclimenes yucatanicus), the shrimp Periclimenes rathbunae, the shrimp Thor amboinensis, the arrow crab Stenorhynchus seticornis, the anemone crab Mithraculus cinctimanus and a brittle star. 6.7 Family Aliciidae 231

Envenomation: The nematocysts of this toxic and stinging anemone are powerful enough to sting a human (Anon. http://www.globetrotterscience.com/uploads/2/1/8/ 4/21849914/ms_chapter_8.pdf).

Phyllodiscus semoni Kwietniewski, 1897

Image credit: Bert W. Hoeksema and Andrea L. Crowther—Bert W. Hoeksema and Andrea L. Crowthe, Wikipedia Common name (s): Night anemone, sea wasp anemone Global distribution: Tropical, western central Pacific: Philippines. Ecology: This sessile species inhabits reef fronts, reef backs and lagoons. Biology Description: This species presents a sponge-like appearance during daytime, and at night forms a white column with long tentacles. Retracted into a fuzzy mass of irregular tentacles, it looks like some sort of variably coloured clump of algae. Envenomation: Prentis et al. (2018) and (Goemans 2012a) reported that this species is dangerous to humans, with severe reactions observed following contact with it. It can inflict a painful and very serious sting and most injuries caused by this sea anemones are associated with skin rashes and oedema. Anon. (http://www.underwaterkwaj.com/uw-misc/coral/Phyllodiscus/Phyllodiscus- semoni.htm) reported that the extremely powerful and potentially dangerous sting of this species can cause inflammation and long-term discolouration, and it has caused a human death in the Philippines. Further it targets the kidney and can cause severe renal injury. Mizuno et al. (2007, 2012) reported that the envenomation by the sea anemone has caused fulminant dermatitis and, rarely, acute renal failure in humans. Its toxins viz. PsTX-T and PsTX-115 were found to be highly nephrotoxic acting via induction of complement activation. Nagai et al. (2002) reported that this species has caused cases of severe stinging. The toxin PsTX-20A, which is a haemolytic and lethal polypeptide (20 kDa), from 232 6 Biology and Ecology of the Venomous Marine Anthozoans (Class Anthozoa) the nematocyst venom of this species showed lethal toxicity to the shrimp Palaemon paucidens when administered via intraperitoneal injection and haemolytic activity towards sheep red blood cells. Anon. (https://www.uniprot.org/uniprot/P58911) reported on the isolation of a toxin DELTA-alicitoxin-Pse2a in this species. Frazão et al. (2012) reported on the isolation of cytolysins Pstx-20A, PsTX-60A and PsTX-60B and nephrotoxin PsTX-115 from this species. DELTA-alicitoxin-Pse2a (https://www.uniprot.org/uniprot/P58911).

Triactis producta Klunzinger, 1877

Image credit: Wikimedia Commons Common name (s): Boxer crab anemone, prolific anemone Global distribution: Tropical Indo-Pacific: from the Red Sea and East Africa to Hawaii and French Polynesia; South of Japan to Australia. Ecology: These anemones are commonly found in shallow reefs, crevices, ledges, between rubble and on fire corals or stony corals, in a depth range of 0–15 m. Biology Description: These anemones are generally small, with a pedal disc diameter of 10 mm or less, and column height of 15 mm when fully expanded. At the top there is a crown with about 50 long tentacles. Most commonly, these anemones are found in closely packed aggregations of presumably clonal individuals. Specimens of this species have evolved specialized column morphology to house dense numbers of pseudotentacles which are hollow, branched outpocketings of the column wall. They are usually dark brown due to the density of the symbiotic zooxanthellae. The posture of this species differs depending on the presence of light. When there is light, the pseudotentacles are expanded, therefore exposing the zooxanthellae to the light to photosynthesize while the true tentacles are retracted. In the absence of light, at night for instance, the true tentacles are expanded and the sea anemone can 6.8 Family Andvakiidae 233 actively feed. Associated with the pseudotentacles is a second specialized feature— the vesicle. The vesicles are spherical bumps that are dense with nematocysts (stinging capsules) on the pseudotentacles. They can be grey, pink or green spherical protrusions on the brown pseudotentacles. Food and feeding: This species can feed in two different ways. With its tentacles retracted and its pseudotentacles extended, it can photosynthesize by the zooxanthellae in the brown algae within. But at night, it can actively hunt for small invertebrates with its tentacles, packed with a powerful toxin. The toxin is strong enough to paralyse the victims, allowing the anemone to eat. Life cycle: The anemone can reproduce by asexual cloning. Association: These anemones are symbiotic with zooxanthellae. Crabs of the genus Lybia (also called boxing or pom-pom crabs) establish a mutualistic association with this species. It is also symbiotic with the boxer crab Lybia leptochelis. Juvenile anemones are used by the crab to cover its claws, for protection and stinging attacks. The anemone benefits by feeding along with the crab. Envenomation: In the Red Sea, this species is reported to be one of the most venomous sea anemones. The symptoms of stings to bare skin include pain and swelling. In one reported case, these lasted for several weeks and were accompanied by a pigmented, blistered lesion and prolonged skin sensitivity (Levy et al. 1971; Anon. https://en.wikipedia.org/wiki/Triactis). Prentis et al. (2018) and Anon. (https://www.marinelifephotography.com/marine/ cnidaria/triactis-producta.htm) reported that this species delivers a painful sting and is dangerous to humans, with severe reactions.

6.8 Family Andvakiidae

Telmatactis australiensis Carlgren, 1950

Common name (s): Club-tipped anemone Global distribution: Great Barrier Reef, Australia. 234 6 Biology and Ecology of the Venomous Marine Anthozoans (Class Anthozoa)

Ecology: It dwells mainly on sandy (inner reef) zone. Biology Description: Column of this species is divisible into scapus covered with a ﬁne cuticle and scapulas. There are 50 tentacles (6 + 6 + 12 + 24 + 2) which are furrowed longitudinally and provided with a swollen apex. Mesenteries in 25 pairs are seen. This anemone is of 13 mm height and of 11 mm diameter. Envenomation: Prentis et al. (2018) reported that the sting of this species was found associated with very severe skin rashes and oedema.

Telmatactis decora (Hemprich & Ehrenberg in Ehrenberg, 1834) (¼ Sagartia longa)

Image credit: Flickr Common name (s): Not designated Global distribution: Tropical, Indo-Paciﬁc; India: Andaman and Nicobar Islands; Maldives and Seychelles. Ecology: This benthic species is usually seen with its oral disk peeking out from under rocks, dead corals or from rocky crevices; depth range, 0–6m. Biology Description: Oral disc is very small and mouth is present on the cone which occupies 2/3 of oral disc. There are two types of tentacles in this species: big tentacles arranged near to cone and the small ones occurred in outer. All the tentacles 6.9 Family Corallimorphidae 235 are thick and their blunt tips are forming bulbs. From the base to middle of the tentacles, it is white in colour and remaining parts are coloured with irregular brown stripes. Base of the tentacles is brownish grey in colour. Column is long with prominent verrucae and is brown in colour. Envenomation: It is a venomous species (Blaxter et al. 1984) and its toxic effects are to be known.

6.9 Family Corallimorphidae

Corynactis australis Haddon & Duerden, 1896

Image credit: Julian Finn, Museums Victoria Common name (s): Southern jewel anemone Global distribution: South-eastern Australia. Ecology: It is found in coastal waters, on reefs and shores, also on rocks and coastal structures such as piers in shaded, wave-exposed areas. Often large colonies of this species cover the walls of underwater caves, with sheets of polyps connected by a single base. Biology Description: Tentacles of the anemone-like polyps of this species have a small round ball at the tip that is usually more brightly coloured than the rest of the polyp, resembling a jewel. Edge of a colony is usually clearly deﬁned as adjoining colonies are often a different colour. Size of the colony is 1.5 cm. Envenomation: It is a venomous species (Marsh and Slack-Smith 2010) and its toxic effects are to be known. 236 6 Biology and Ecology of the Venomous Marine Anthozoans (Class Anthozoa)

6.10 Family Diaduminidae

Diadumene cincta Stephenson, 1925

Image credit: Flickr Common name (s): Orange anemone Global distribution: It is native to the north-eastern Atlantic Ocean: southern North Sea, Britain and western coast of France. Ecology: It occurs in the lower littoral zone and the shallow sublittoral zone down to 40 m; frequently found in pools and caves; and is found attached to hard substrates, such as rock, mussels or other bivalves. Biology Description: It is a slender, delicate, cylindrical anemone. It grows to 35 mm in length when fully expanded, with a basal width of 10 mm. Base is slightly wider than the column. Lower part of the column is opaque and is separated from the translucent upper part by a small ledge and groove. Oral disc is no wider than the column and has a central mouth surrounded by up to 200 long, slender tentacles. This sea anemone is orange in colour, sometimes with a greenish tinge, but some populations are fawn. Some of the tentacles are thicker and longer than normal tentacles and are known as catch tentacles which are common in some populations but absent in others. Food and feeding: Like other sea anemones, it is a predator. It is catching the prey with its tentacles and immobilizing it with its stinging cells. The tentacles then bend to pass the food into the mouth. 6.10 Family Diaduminidae 237

Life cycle: This species reproduces by basal laceration. As the animal moves on its base across the substrate, a chunk of tissue becomes detached and in time develops into a new individual. This basal laceration is habitual and frequent. Association: It is dominant along with the breadcrumb sponge Halichondria panicea and the cave-dwelling anemone Sagartia troglodytes Envenomation: It is a venomous species (Blaxter et al. 1984) and its toxic effects are to be known.

Diadumene lineata (Verrill, 1869) (¼ Aiptasiomorpha (Diadumene) luciae; Haliplanella lineata)

Image credit: WoRMS Common name (s): Orange-striped green sea anemone Global distribution: Pacific coast of Asia; Northern Hemisphere; Japan, Gulf of Mexico, Plymouth and Wells, Norfolk, England, Western Europe, Mediterranean Sea, Suez Canal, Malaysia; North America on the East Coast from Maine to Florida; Hawaii; Argentina and other localities of South America. Ecology: This extremely euryhaline and eurythermal species is found attached to ship bottoms, oyster shipments and seaweed in subtidal waters, including shallowly buried rocks in mudflats and marsh channels. It is also found in salt marshes in estuaries and are found attached to roots and stems of the mangrove pant, Spartina alterniflora. It is a member of the fouling community but does not cause significant economic impacts. It displays high tolerance to intertidal exposure and drying out in extreme summer heat. It forms encystments when locked in freezing climates. It also acclimatizes to severely low salinities. Biology Description: This is a smaller species, measuring 3.5 cm in diameter across its tentacles and 3 cm in height. Its central column is greenish grey to brown colour and 238 6 Biology and Ecology of the Venomous Marine Anthozoans (Class Anthozoa) smooth. Its column, which houses the gastrovascular central cavity, extends from the mouth to the attached base called the pedal disc. There are 50–100 slender and tapered tentacles which are able to retract completely into the column. They are commonly transparent and can be grey or light green with white flecks. Many morphs occur for this species. Food and feeding: The nematocysts are found on both catch tentacles and feeding tentacles of this species. The catch tentacles used for aggression and capturing of prey have larger length and width than feeding tentacles, which aid in the capture of food. Life cycle: While this sea anemone can reproduce sexually, it normally reproduces asexually by longitudinal fission. In the asexual process, a new polyp develops from a portion of the original polyp after pulling away (anemone splits in half). Envenomation: It is a venomous species (Russell 1965) and its toxic effects are to be known.

Diadumene leucolena (Verrill, 1866)

Image credit: Flickr Common name (s): White anemone, ghost anemone Global distribution: Subtropical; western Atlantic and eastern Pacific: Mexico, USA and Canada; north-eastern Atlantic Ocean, Caribbean Sea and northern Pacific Ocean. Ecology: This sessile species is a shallow water species occurring in intertidal and subtidal areas; in bays and areas of low salinity; and on stones, shells of live oysters and man-made structures such as pilings and floats. 6.10 Family Diaduminidae 239

Biology Description: When fully extended, this solitary anemone has a long and slender column which is up to 38 mm tall and 12 mm wide. Both column and tentacles are a translucent pale pink or flesh colour; and column sometimes is having a faint green tinge near the top. Column appears to be smooth but on close inspection, it shows irregularly arranged darker swellings. Tentacles closest to either end of the mouth have yellow bases. Food and feeding: It eats plankton and tiny fish, using its stinging tentacles to stun and capture its prey. Predators: The nudibranchs, Cuthona perca and Hermissenda crassicornis, eat this species. Life cycle: It reproduces sexually and asexually. In sexual reproduction, males and females liberate their gametes into the sea. After fertilization, it takes 18 h for the embryo to develop into a swimming planula larva. These larvae which are ciliated and have an apical tuft on their aboral end disperse, settle on the seabed, undergo metamorphosis and develop into new individuals. Asexual reproduction is by longitudinal fission of the column or pedal laceration. Associates: These anemones are found living with the plumose anemone, Metridium sp.; also found on the mussel Mytilus edulis with its accompanying fauna; and are growing on the stems and roots of the cordgrass, Spartina alterniflora. Envenomation: The catch tentacles of this species are used only for stinging (Anon. https://scholarsbank.uoregon.edu/xmlui/bitstream/handle/1794/12640/D_ lineata_2015_final.pdf?sequence¼3). Macrander and Daly (2016) reported on the presence of cytolytic proteins actinoporins from the venom of this species. 240 6 Biology and Ecology of the Venomous Marine Anthozoans (Class Anthozoa)

6.11 Family Discosomidae

Amplexidiscus fenestrafer Dunn & Hamner, 1980

Common name (s): Elephant ear mushroom, giant cup mushroom Global distribution: Tropical Indo-Pacific Ocean: from Mayotte and the Maldives in the west to French Polynesia in the east, and from southern Japan to New Caledonia. Ecology: This species prefers slightly turbid waters. It is found in lagoons, coral reefs, seagrass beds, rocky bottoms or rich in coral debris at depths of 1–30 m. Biology Description: This species is in the shape of a thin and flexible disc; up to 90 cm in diameter; and it is attached to the substrate by a large foot. Edges of the disc are generally raised giving this species the appearance of a plate or a pie dish. Interior of the greenish brown oral disc is lined with short fleshy tentacles which are fleshy and greenish in colour. These tentacles are arranged in concentric circles and at the same time form radiating lines from the mouth. Food and feeding: This anemone will actively eat fish if they are available by forming a ball around them. It also receives some of its nutritional requirements from the symbiotic algae zooxanthellae. Life cycle: This anemone is hermaphroditic. It reproduces typically by pedal laceration or budding, but fission is occasional. Envenomation: It is reported that in the western Indo-Pacific, the stinging tentacles of this most dangerous species can penetrate wetsuits causing significant pain. Initial symptoms vary from a prickly sensation to severe pain. The afflicted area can become red, swollen and blistered (Bowles et al. 2018). 6.11 Family Discosomidae 241

Rhodactis howesii Saville-Kent, 1893

Image credit: Gustav Paulay Common name (s): Green fuzzy mushroom, elephant ear mushroom coral, giant anemone, giant mushroom anemone and giant cup mushroom. Global distribution: Tropical Pacific Ocean. Ecology: It is a coral reef-associated species. Biology Description: This species is essentially a coral without a skeleton and its internal structure is similar to a stony coral. Its upper surface is the oral disc. It has a short stalk or column below which is the pedal disc which adheres to the substrate. It can detach itself and drift to another location. It is either green or brown, and 5–8cmin height. Tentacles are very short and somewhat knobbly, giving the oral disc a fuzzy appearance. Tentacles at the edge of the disc are longer. Food and feeding: It is a carnivore catching plankton and other micro particles that float past its oral disc. It also obtains nutriments from its endosymbiotic algae Life cycle: It reproduces sexually and asexually. There are three asexual means of reproduction in this species. Budding can occur when new individuals are formed from pieces that divide off from the pedal disc. Fragmentation can occur when the individual moves slowly over the substrate and leaves its small pieces which eventually grow into new individuals. Division or fission can also occur when the corallimorph divides down the centre to form two new individuals. Sexual reproduction also sometimes occurs, and eggs and sperm are released into the water. They unite and form free-swimming larvae which are initially planktonic. Later they settle and adhere to the substrate, growing into new individuals. Envenomation: The stings of this species are not harmful to humans. However, this species is toxic when it is eaten raw and ingestion can cause fatal poisoning. The death of the victim is largely due to prolonged shock and associated death from pulmonary oedema (the filling of the lungs with fluid) (Anon. https://en.wikipedia. org/wiki/Rhodactis_howesii). However, cooking in water destroys the poison and cooked animal is commonly eaten by the natives. 242 6 Biology and Ecology of the Venomous Marine Anthozoans (Class Anthozoa)

Martin (https://pdfs.semanticscholar.org/1cd5/465eee4f32ed5e040f547b1cefab3 1099809.pdf) reported that the toxins of this species may be due to one or the other of the following: its own tissue metabolism; the metabolism of a symbiont which lives in the tissue of the invertebrate; and the ingestion of poisonous plankton. Martin (1960) also reported that the toxin of this species was lethal to just about every vertebrate he injected it into: salamanders, toads, mice, rats, rabbits. To kill a mouse within 4 h requires just 3 mg/kg of weight. Its toxin was acting primarily on the central nervous system.

6.12 Family Edwardsiidae

Edwardsiella lineata (Verrill, 1873)

Image credit: WoRMS Common name (s): Lined anemone Global distribution: It is native to temperate waters in the north-western Atlantic Ocean, where it occurs between Cape Cod and Cape Hatteras. Ecology: It occurs in rock crevices and on and under rocks in the shallow subtidal zone at depths to 20 m and can also be infaunal, burrowing in soft sediment. Description: It is a small, delicate-looking, white or brownish anemone with a length of up to 3.3 cm. It has 40 tentacles and acontia (thread-like defensive organs thrown out of the mouth or special pores when irritated). Life cycle: This species reproduces sexually and asexually. In sexual reproduction, the evolved planula larva has a partially parasitic lifestyle. The host is the pelagic ctenophore, Mnemiopsis leidyi. On entering a host, the larva adopts a worm- like appearance and feeds on the contents of the host’s gut. When the larva is fully developed, or if the host dies, it exits the host and regains its planula larval form. If another host is available, it can once again adopt the worm-like phase, but if no new host is available, it can settle on the seabed and undergo metamorphosis into a juvenile sea anemone (polyp). 6.12 Family Edwardsiidae 243

Envenomation: The planula larvae of this species are sometimes the cause of a form of irritating dermatitis in humans known as “seabather’s eruption”. When the larvae get trapped under swimwear, they defend themselves by ﬁring their venomous nematocysts into the skin, causing a red blotchy rash that may blister (Anon. https:// en.wikipedia.org/wiki/Edwardsiella_lineata). Schmitt and de Haro (2013) reported that the seabathers’ eruption (lesions) caused by the planulae of this species may be accompanied by systemic symptoms, e.g. fever, headache, muscle pain and nausea, in the acute phase and can progress to pigmented lichenoid dermatitis or chronic granulomatous lesions resembling prurigo.

Nematostella vectensis Stephenson, 1935

Image credit: Smithsonian Environmental Research Center, Wikipedia Common name (s): Starlet sea anemone Global distribution: Native to the east coast of the United States; introduced along the coast of south-east England and the west coast of the United States; eastern and westward seaboard of North America; extends from Nova Scotia to Louisiana on the east coast and from Washington to California on the west coast; Canada. Ecology: This sea anemone is found in the shallow brackish water of coastal lagoons and salt marshes where its slender column is usually buried in the mud and its tentacles are exposed. Biology Description: This sea anemone has a bulbous basal end and a contracting column that ranges in length from less than 2 to 6 cm. There is a fairly distinct division between the scapus, the main part of the column, and the capitulum, the part just 244 6 Biology and Ecology of the Venomous Marine Anthozoans (Class Anthozoa) below the crown of tentacles. Outer surface of the column has a loose covering of mucus to which particles of sediment tend to adhere. At the top of the column is an oral disk containing the mouth surrounded by two rings of long slender tentacles. There are 14–20 tentacles and outermost tentacles are longer than the inner whorl. It is translucent and largely colourless but usually has a pattern of white markings on the column and white banding on the tentacles. Food and feeding: It feeds on ostracods, copepods, small molluscs, chironomid larvae, nematodes, polychaetes, small crustaceans and egg masses. Predators: The only known predator of this sea anemone is the grass shrimp Palaemonetes pugio. Life cycle: On the east coast of the United States, reproduction of this species is mostly by sexual means. These anemones get matured in 3–4 months when it has a column length of 2 cm or more. It lays about 2000 eggs in a gelatinous clump. The resulting spherical planula larvae spend around a week in the water column before settling on the sediment and undergoing metamorphosis into juveniles. In southern England, all individuals of this species seem to be female and reproduction is by budding. Two-crowned anemones are common in this location and these individuals later undergo ﬁssion into separate sea anemones. On the west coast of the United States, all individuals are also female, while in Nova Scotia, all are male, and reproduction in both these populations is mainly by asexual means. Envenomation: Columbus-Shenkar et al. (2018), Frazão et al. (2012) and Jouiaei et al. (2015a) reported that the stinging cells appear in the planulae larvae of this species. These larvae are venomous and their neurotoxin is capable of rapidly killing a crustacean that is larger than they are. Frazão et al. (2012) reported that this species contains a variety of neurotoxins, NaV channel toxins such as Nv1-116.25.1, Nv1-116.27.1, Nv1-116.28.1, Nv1-116.37.1, Nv1-116.39.1, Nv1-116.40.1, Nv1-116.41.1 and Nv1-116.45.1. 6.13 Family Exocoelactinidae 245

6.13 Family Exocoelactinidae

Exocoelactis actinostoloides (Wassilieff, 1908) (¼ Parasicyonis actinostoloides)

Image credit: Yanagi, Fujii, and Hirose, The Japanese Society of Systematic Zool- ogy, 2015 Common name (s): Not designated Global distribution: Tropical western Paciﬁc: Japan, New Caledonia, Palau, the Philippines and Somali Peninsula. Ecology: It is a fairly deep-water species occurring at depths of 175–823 m. Biology Description: It is typically ﬂat and some individuals are with many shallow, radial furrows. Column of this species has creamy white oral disc and is with narrow orange radial stripes on light orange background. Tentacles are of same colour as oral disc and they have background colour proximally and orange distally. Oral side of tentacles is slightly darker coloured than aboral side. In living, expanded animal, column height is 70 mm; oral disc diameter is 150 mm, and pedal disc diameter is 65 mm. Some individuals have radially aligned ovoid holes on oral disc where tentacles have been cast or plucked off. Pedal disc is weakly adherent and is circular in outline. Scapus is smooth, with no distinct margin or fosse. Mouth in most specimens is slit-like to ovoid, and in some it is raised on cone. There are 108 tentacles; marginal tentacles are, short, more or less capitate, simple and are shorter than oral disc diameter; and inner ones are longer than outer ones. Two siphonoglyphs are distinct. Diameter of the anemone may vary from 30 to 200 mm. Life cycle: Envenomation: The toxin from this species has been reported to inhibit the inactivation process of the sodium channel (Fujita et al. 1983). Frazão et al. (2012) reported on the presence of a NaV channel toxin PA-TX from this species. 246 6 Biology and Ecology of the Venomous Marine Anthozoans (Class Anthozoa)

6.14 Family Gorgoniidae

Leptogorgia rigida Verrill, 1864 (¼ Lophogorgia rigida)

Image credit: WoRMS Common name (s): Not designated Global distribution: Tropical, Eastern Paciﬁc; Costa Rica, El Salvador, Mexico and Panama. Ecology: It is a benthic species, with a depth range of 5–30 m. Biology Description: It is a dark bluish purple colony with 22.5 cm in height and 13.5 cm in width. Three main branches arise in various planes from a thick stem which is 60 mm in diameter and 40 mm in length. Branches are slightly ﬂattened at the base, 8–9 mm in diameter and are with distinct longitudinal grooves. Branching is pinnate, producing pinnae of 2.0–3.0 mm in diameter that are irregularly arranged and are separated by short distances (around 10–20 mm). These pinnae also rebranch giving off secondary pinnae which are up to 1–1.5 mm in diameter and are with somewhat enlarged and blunt ends. Unbranched terminal twigs reach up to 30 mm in length. Polyps are retracted within slightly raised dome-shaped polyp mounds with small oval apertures (around 0.2 mm). Polyp mounds are distributed all around the 6.15 Family Halcuriidae 247 branches and do not crowd the branches. They are closer together on the large branches and are arranged in three to four longitudinal rows with naked median spaces alongside of the median grooves. Envenomation: A neuromuscular toxin lophotoxin has been isolated from this species (Culver and Jacobs 1981; Fenical et al. 1981).

Lophotoxin

6.15 Family Halcuriidae

Halcurias carlgreni McMurrich, 1901 248 6 Biology and Ecology of the Venomous Marine Anthozoans (Class Anthozoa)

Image credit: Flickr Common name (s): Gloﬁsh Global distribution: Tropical; northwest Paciﬁc; Japan. Ecology: This benthic species is found in deeper cool waters. Biology Description: Body of this species is elongated. Column is almost smooth, sometimes with longitudinal and horizontal striate. Few small nematocyst batteries are found scattered on the distal part. Distal margin of column is tentaculate. Nematocyst batteries of column with many spirocysts of stout type and many basitrichs. Tentacles are up to 68 in number, and each tentacle is much longer comparing with its body size. Column is orange in shallow water individuals and is white with many small specks of orange red in colour in deep-water ones. Food and feeding: It is a meat-eating anemone. Envenomation: Jouiaei et al. (2015a) and Frazão et al. (2012) reported on the presence of a neurotoxin (NaV channel toxin) halcurin from this species. This polypeptide toxin is lethal to crabs.

Halcurias minimus Carlgren, 1928 Image not available Common name (s): Not designated Global distribution: Circum-antiboreal region. Ecology: It lives in rather deep water. Biology Description: Tentacles of this species are not so long and are with two sorts of basitrichs. Ectoderm of column is with sparse spirocysts. Envenomation: Mariottini (2014) reported that the venom of this species has shown haemolytic activity. 6.16 Family Hormathiidae 249

6.16 Family Hormathiidae

Adamsia palliata (Muller, 1776) (¼ Adamsia carcinoapados)

Common name (s): Cloak anemone, hermit crab anemone Global distribution: North-east Atlantic Ocean; Azores, North Sea and Mediterra nean Sea. Ecology: It occurs in deep water (30–40 m) on sandy flats and particularly favours muddy gravelly bottoms with shell fragments. It is usually found growing on a gastropod shell inhabited by the hermit crab, Pagurus prideaux. This anemone often completely envelops the shell. Biology Description: Anemone’s base is wide and convoluted with lobes that extend around the shell. Its edges join together in a suture where the shell is completely encircled. Oral disc and tentacles are orientated downwards beneath the underside of the crab. Basal lobes extend to 15 cm while trunk is only about 1 cm high. Column is fawn and is tinged with pinkish purple; and is paling to white near the parapet. It is covered with vivid magenta spots which are largest in the central portion. There is a narrow pink line round the margin of the parapet and the oral disc and tentacles are white. Tentacles are numerous, 1 cm long, not fully retractable and are arranged in four sub-marginal rows. Mouth is long, oval and it protrudes from the disc. When it becomes too large for the shell, the anemone secretes a chitinous membrane at its base. This has the effect of increasing the volume of the shell available to the hermit crab which can then inhabit it for a longer period. On the lower part of the column, there are special cells which emit defensive pink (occasionally white) threads called acontia if and when the animal is disturbed. Life cycle: It breeds during the summer months. Several hundred globular golden eggs are ejected into the water column through the mouth and are fertilized externally. Each egg develops into a planula larva which settles and develops into a 250 6 Biology and Ecology of the Venomous Marine Anthozoans (Class Anthozoa) juvenile sea anemone. This larva is drawn to settle on the inner lip of a gastropod shell. At first, the larva develops in the same way as a typical sea anemone, but as it grows, its base extends around the gastropod shell until the two lobes meet at the upper side of the lip. Association: The symbiosis between this species and hermit crab Pagurus prideaux is beneficial to both the animals. Envenomation: Talvinen and Nevalainen (2002) and Frazão et al. (2012) reported on the presence of a toxin AcPLA from the venom of its body, tentacles and acontia of this species. This toxin which contains a putative prepropeptide plays crucial roles in diverse cellular responses, including phospholipid digestion and metabolism, host defence and signal transduction.

Calliactis parasitica (Couch, 1844)

Image credit: Wikimedia Commons Common name (s): Parasitic anemone Global distribution: Subtropical eastern Atlantic Ocean and Mediterranean Sea; Atlantic range extends from south-western Europe as far north as the west coasts of Wales and Ireland, and the English Channel. Ecology: This sessile species is found at depths between the intertidal zone and 60 m; sessile. Biology Description: This anemone is up to 100 mm tall and 80 mm wide, with the base of the column slightly wider. Surface of the column is rough and leathery with a grainy appearance, but it has no tubercles and is not divided into sections. It is variable in colouration but is usually cream or buff in colour, with blotches and streaks of reddish or greyish brown, which tend to form vertical stripes. Basal disc is concave and is able to stick ﬁrmly to the substrate. Above this lies the limbus (the junction between the basal disc and the column), and just above that are the relatively 6.16 Family Hormathiidae 251 prominent cinclides (specialized pores), each on a small mound. These readily emit thread-like acontia (stings) when the animal is disturbed. At the top of the column, there are up to 700 slender tentacles of moderate length. They are translucent and yellowish to orange in colour, with longitudinal lines of reddish brown in colour. Association: The relationship between this anemone and the hermit crab (Pagurus bernhardus)ismutualistic. While the sea anemone protects the hermit crab with its stings, the anemone is beneﬁtted from the food thrown up by the hermit crab’s movements. Envenomation: Shiomi et al. (1997), Frazão et al. (2012) and Cariello et al. (1989) reported that the polypeptide toxin (neurotoxin, sodium channel toxin) calitoxin (CLX) has been isolated from this species.

Calliactis polypus (Forsskal, 1775)

Image credit: Wikimedia commons Common name (s): Outer-hermit sea anemone Global distribution: Subtropical; Indo-West Paciﬁc; Red Sea. Ecology: This benthic species lives on the surface of a sea snail shell in which a hermit crab is living; several anemones of this species can grow on one shell and in the neritic zone at depths down to 25 m. Biology 252 6 Biology and Ecology of the Venomous Marine Anthozoans (Class Anthozoa)

Description: It can grow up to 8 cm long. Base is wide with wavy edges and pink striations and ﬂares out over the shell surface. Column is wider at the base than further up and has pale brown and white patches and longitudinal striations. Oral disc has several whorls of long brownish translucent tentacles with paler bases surrounding the mouth. Association: It lives as a commensal with several species of hermit crab including Dardanus gemmatus. Envenomation: Yamaguchi et al. (2010) reported that this species has Kv1 potassium channel toxicity.

6.17 Family Metridiidae

Metridium senile (Linnaeus, 1761)

Image credit: Flickr Common name (s): Frilled anemone Global distribution: North-western Europe: from the Bay of Biscay north to Norway and Iceland; both the east and west coasts of North America and has arrived in South African waters. Ecology: It is found on the lower shore and the neritic zone at depths down to about 100 m. It adheres to rocks, boulders, man-made structures, pebbles and shells. It favours areas where the current is strong. Smaller forms inhabit the lower shore under stones, beneath overhangs and in shaded places. It specially favours soft rocks, honeycombed by molluscs, and the underside of large boulders. At greater depths, 6.17 Family Metridiidae 253 the larger forms are sometimes abundant on pilings, submerged pipes, pier supports and harbour walls. Biology Description: Base of this anemone is considerably wider than the column which is long, smooth and cylindrical, and of a fleshy consistency with a slimy surface lubricated with mucus. There are no warts or suckers, and the column is topped by a parapet and deep groove. Oral disc is broad and deeply lobed into several curving sections that overhang the column. Its slender, pointed tentacles are very numerous in larger specimens though fewer and relatively longer in smaller ones. Those tentacles near the margin are crowded and short, whereas further into the disc they are longer and more dispersed. Colour range of this sea anemone is large and these colours include white, cream, pink, orange, red, grey, brown and olive green. Tentacles are translucent but may have a white band. Some specimens have a darker column and much paler disc. There are several distinct forms and various intermediate ones. M. senile var. dianthus which is described above has over 1000 tentacles, and it exhibits a feathery appearance. It can grow to 30 cm tall with a base diameter of 15 cm and a similar tentacle span. M. senile var. pallidus is much smaller, seldom exceeding 2.5 cm base diameter and has a much less convoluted disc with fewer than 200 tentacles. There are also a number of intermediate forms. Food and feeding: Its diet largely consists of copepods, worm larvae, mollusc larvae, ascidian larvae, amphipods and barnacle larvae. Predators: The sea slug Aeolidia papillosa (“shag rug nudibranch”), the sea spider Pycnogonum littorale, wentletrap sea snails Epitonium spp., the flounder Pseudopleuronectes americanus and the black bream Spondyliosoma cantharus. Life cycle: It is a protandric hermaphrodite and it starts life as one sex and changes to the other when it is older. Eggs or sperm develop in the gonads and are embedded in the mesentery that lines the coelom. They are ejected through the mouth, and when fertilized develop into planula larvae. After 1–6 months drifting in the plankton, these settle and metamorphose into juveniles. This anemone can also increase its numbers by asexual reproduction. An individual can undergo binary fission by splitting in half and growing into two organisms. Or it can develop buds which grow into new individuals before they are detached. Fragmentation, also known as basal laceration, is another method of asexual reproduction by which the number of individuals can be increased rapidly. Envenomation: Frazão et al. (2012) reported that the Kv channel toxin metridin has been isolated from the venom of this species. Maček (1992) reported on the presence of a toxin metridiolysin from this species. This toxin has been reported to possess cardiotoxic, cutolytic and cytotoxic properties and is lethal for both invertebrates and vertebrates. Anderluh and Macek (2012) reported on the presence of cytolytic peptide and protein toxins (cytolysins) from this species. 254 6 Biology and Ecology of the Venomous Marine Anthozoans (Class Anthozoa)

6.18 Family Nephtheidae

Dendronephthea sp.

Image credit: Wikimedia Commons Common name (s): Soft coral Global distribution: Indo-Paciﬁc: Tonga; Solomon Islands to Great Barrier Reef in Australia. Ecology: It grows in various parts of the reef. It is normally found upside down in caves and other sheltered areas of the reef, yet some species are also found in sunny areas. Biology Description: It is a ﬂower-shaped soft coral with various formations. It has scratch, like thorn, along its body. These scratches or thorns are sclerites formed by silica layers and play an important role as a supporting bundle. Life cycle: In the natural habitat, this species grows and breeds rapidly. Association: Dendronephthya sp. has an association or symbiotic relationship with several bacteria such as Actinobacteria, Arthrobacteria, Chlorobia, Caldilineae, δ-proteobacteria and Proteobacteria which are commonly known as coral-associated bacteria. 6.18 Family Nephtheidae 255

Envenomation: This species has been reported to sting humans. Nematocyst venoms of this species is lethal to mice and haemolytic to human erythrocytes (Radwan et al. 2002). Suput (2011) reported that the pro-inﬂammatory proteins isolated from the nematocyst venom of this species caused dermonecrosis and oedema when injected locally in sub-lethal concentrations.

Litophyton sp. (¼ Nephthya sp.)

Image credit: Nick Hobgood, Wikipedia Common name (s): Soft coral Global distribution: Widespread in tropical Indo-Paciﬁc. Ecology: It is a shallow water species. Biology Description: Colonies of this species are arborescent with branched polyparium. Polyps are arranged in catkins on the terminal branches only and are not retractile. Sclerites of this species are spindles and are unilateral spinose spindles. Surface layer of base of stalk is also with capstans and derivations of capstans. Colour of colonies is whitish, pink or brownish. Zooxanthellae are present. Envenomation: This species has been reported to sting humans. Nematocyst venoms of this species is lethal to mice and haemolytic to human erythrocytes (Radwan et al. 2002). 256 6 Biology and Ecology of the Venomous Marine Anthozoans (Class Anthozoa)

Suput (2011) reported that the pro-inﬂammatory proteins isolated from the nematocyst venom of this species caused dermonecrosis and oedema when injected locally in sub-lethal concentrations. Mariottini and Pane (2014) reported that the eunicellin-type diterpenoids litophynols A and B, litophynins E and H, and I monoacetate isolated from the mucus of this species were found to have haemolytic properties on a 2% rabbit erythrocyte suspension.

6.19 Family Parazoanthidae

Parazoanthus axinellae (Schmidt, 1862)

Image credit: Dr. Luis Sánchez Tocino Common name (s): Yellow cluster anemone Global distribution: Temperate eastern Atlantic Ocean; southern Atlantic coasts of Europe and Mediterranean Sea. Ecology: It occurs on rocky substrates at depths between 23 and 45 m. Biology Description: colonies of this species are yellow or orange in colour and each polyp has 24–36 tentacles arranged in two whorls. Polyps are 5 mm in diameter and 20 mm in height. They are connected together in small colonies by a continuous layer of tissue, the coenenchyme. In this species there are sometimes thick yellow spongy masses of tissue at the base of each zooid. Envenomation: Turk et al. (1995) reported that the ethanolic extract of this species exhibited anticholinesterase activity (acetylcholinesterase (AChE) stops the signal between a nerve cell and a muscle cell) and was lethal to mice and crabs.

Parazoanthus sp. Envenomation: Hoffmann et al. (2008) reported that the palytoxin of this species caused skin injuries on ﬁngers on contact. The associated clinical symptoms include swelling, paraesthesia and numbness around the site of the injury spreading over the arm, and also signs of systemic poisoning such as dizziness, general weakness and myalgia, irregularities in the ECG and indications of rhabdomyolysis. 6.20 Family Phymanthidae 257

Raghubir et al. (2013) reported on the presence of a potent neurotoxin in the methanolic extract of this species.

6.20 Family Phymanthidae

Phymanthus crucifer (Le Sueur, 1817)

Common name (s): Red beaded anemone; beaded, rock, flower or speckled anemone Global distribution: Caribbean Sea across the West Indies. Ecology: This species can adhere to vertical shaded walls, or rocky ledges where they can withdraw into crevices upon agitation; and found in coral reefs or buried in the ocean floor at depths of 1–5m. Biology Description: This anemone has a range of colour from a grey-green to a chestnut brown. However, this species is mostly known for its tentacles and beaded appearance which is due to white spots (clusters of stinging cells or nematocysts) that grow randomly into bead-like swellings or run the length of the tentacles making the anemone appears ornamental with red suckers on its column. Its cream-coloured column extends to a pedal disc (“foot”) that is used to root the anemone to a particular spot or move around when desired. Mouth of the anemone is found in the centre; most times the same colour as the disc of the anemone and is usually closed only opening when the anemone is hungry or is used as a warning signal. This anemone ingests food and expels waste via the same opening. This sea anemone has approximately 200 short tentacles and is capable of growing to 15 cm across its column when fully extended, reaching 15–20 cm in length. Food and feeding: It is a carnivore and its diet includes plankton or anything that is caught in its tentacles including big fish, small fish and snails. These anemones 258 6 Biology and Ecology of the Venomous Marine Anthozoans (Class Anthozoa) move around and feed at night. They use the nematocysts in their tentacles to catch their prey as the nematocysts contain tiny barbs with venom that would paralyse their prey and enable them to take the prey into their mouths to feed. Predators: The predators of this anemone are generally sea stars and nudibranchs though they may have a few fish predators. Life cycle: It is a dioecious species (separate male and female individuals). In its sexual reproduction, the fertilized eggs give rise to ciliated planula larvae within the parent and these larvae drop on the ocean floor, develop a pedal disk and grow into juvenile anemones without tentacles. This species can also reproduce asexually via fission. The process of fission happens as the anemone splits to produce a clone. Envenomation: Rodríguez et al. (2018) reported that a paralysing toxin PhcrTx2 has been isolated from this species. Rodríguez et al. (2014) reported that the toxin PhcrTx2 h of this species acted on acid-sensing ion channel (ASIC) toxins.

6.21 Family Plexauridae

Eunicia mammosa Lamaouroux, 1816

Image credit: Quintín Muñoz, Wikipedia Common name (s): Gorgonian-type octocoral Biology Description: These branched octocorals typically have knobby protuberances from which the polyps protrude. They are often stiffened by purple sclerites and some colonies in brightly lit back-reef areas are purple, though most colonies are brown or grey. The polyps in some species are large and feathery in appearance. 6.21 Family Plexauridae 259

Envenomation: Sammarco and Coll (1988) reported on the direct toxic effects of cembranolides derived from this species. Sorokin (1993) reported on the presence of toxic lactones crassin and mammosin from this species.

Eunicia succinea (Pallas, 1766)

Common name (s): Shelf-knob sea rod Global distribution: Bahamas, South Florida and Caribbean Sea. Ecology: It occurs on reef terraces and slopes with moderate wave exposure, from shallow water to 25 m in depth. Biology Description: This species is bushy mainly in one plane with branches arising near colony base. It is up to 1 m tall. Branches are few and are separated to profuse and crowded. These branches are about 7 mm across and are less than 50% colony height. Apertures are hemispherical with lower lip. Its calices are recognized by their diagonally upward protrusion. Rows of calices are sometimes spiral along branches. Colour of the colony is ochre and polyps are light brown. Envenomation: Sammarco and Coll (1988) reported on the direct toxic effects of cembranolides derived from this species. 260 6 Biology and Ecology of the Venomous Marine Anthozoans (Class Anthozoa)

6.22 Family Pocilloporidae

Pocillopora damicornis (Linnaeus, 1758)

Common name (s): Cauliflower coral, lace coral Global distribution: It is native to tropical and subtropical parts of the Indian and Pacific Oceans. Its wide range extends from East Africa and the Red Sea to Japan, Indonesia, Australia, Hawaii, Easter Island and the western coast of Central America. Ecology: It is found on reef slopes and in lagoons, among mangroves and on wharves at depths of 5–40 m. It often forms dense patches. Biology Description: It is a colonial coral and can grow into clumps up to 30 cm high. It has the characteristic verrucae (wart-like growths) which are more irregularly arranged on its surface. Its form varies according to its habitat. It is more open and branched in calm positions and more compact on the upper parts of reefs where water movement is greater. Its colour varies and it may be greenish, pink, yellowish brown or pale brown. Food and feeding: The polyps of this species extend their tentacles at night to feed on plankton. Life cycle: It reproduces both sexually and asexually. In asexual reproduction which is by fragmentation, colonies are broken apart and chunks can become lodged on the seabed and grow into new individuals. It is a simultaneous hermaphrodite, and eggs and sperm are retained inside the coral and batches of planular larvae are released into the sea during new moon. These larvae have great dispersal abilities as they remain viable for as much as 100 days. Larvae after settlement become new individuals. Association: This coral species contains microscopic symbiotic dinoflagellate algae (zooxanthellae) living within its tissues. Envenomation: It causes skin irritation upon contact, and it has been suggested that high levels of PLA2 activity in its venom are responsible for this effect (Suput 2011; Nevalainen et al. 2004). 6.23 Family Sagartiidae 261

6.23 Family Sagartiidae

Sagartia elegans (Dalyell, 1848) (¼ Sagartia rosea)

Image credit: Shutterstock Common name (s): Elegant anemone Global distribution: Northwest Europe; north-east Atlantic Ocean from Scandinavia, Iceland and the North Sea south to the Mediterranean Sea; British Isles and Netherlands. Ecology: It occurs in coastal areas at depths down to 50 m. When not submerged, it hangs in a limp fashion. It sometimes partially protrudes the lining of its coelom through its mouth. If disturbed, it will retract more completely, disappearing from view if it is found in a crevice. It is found from the mid-shore down to a depth of about 50 m in holes and cracks in the rock; also found under stones, beneath overhangs, in rock pools and caves; and favours brightly lit rock walls with fast-moving currents. Biology Description: Base of this species is wider than the column and may reach 3 cm in diameter. Base is usually anchored to the substrate but can be used as a foot for locomotion. It has a ragged outline during fragmentation process. Column is soft and ﬂeshy and varies in shape, from squat to cylindrical or trumpet shaped, and can grow up to 6 cm tall. Lower part of the column is somewhat corrugated, and there are a number of pale-coloured suckers on the upper part to which grit or shell fragments adhere. Disc is saucer-shaped with an undulating margin, and there are up to 200 tentacles arranged irregularly, often arching over the edge. These are mostly about the same length but occasionally there is a much longer one among them. When it is disturbed, a large number of white threads known as acontia are discharged from cells on the column and from the mouth. 262 6 Biology and Ecology of the Venomous Marine Anthozoans (Class Anthozoa)

Food and feeding: It is an omnivore, scavenger and predator. Most of its nourishment comes from the ingestion of small invertebrates which are caught by the tentacles and passed on to its mouth. The undigested fragments are expelled through the mouth. Life cycle: It often reproduces asexually by fragmentation (also known as basal laceration). As it crawls across a rock surface, pieces of its base become detached and grow into new individuals. Envenomation: Sponge gatherers in the Mediterranean Sea are the victims to this species. When they come in contact with the tentacles of these sea anemones, they are affected with burning and itching sensation followed by erythema and blisters, the symptoms of “sponge ﬁshermen’s disease”. Individuals may also experience nausea, vomiting, fever, muscle spasms and collapse (Turk 1999; Anon. https://en. wikipedia.org/wiki/Sagartia_elegans). Mariottini and Pane (2014) and Frazão et al. (2012) reported on the occurrence of acidic actinoporin from this species. Further, its acidic cytolysin Src-I possess haemolytic activity.

6.24 Family Sphenopidae

Palythoa caribaeorum (Duchassaing & Michelotti, 1860) (¼ Palythoa caribbaea)

Image credit: Wikimedia Commons Common name (s): White encrusting zoanthid Global distribution: Throughout the western Atlantic from southern Florida to southern Brazil. Ecology: It inhabits shallow reefs in areas with some water movement, down to 12 m. Biology 6.24 Family Sphenopidae 263

Description: Colonies of this species which are brownish white form thick, incrusting mats on dead corals and other hard substrates. Skeleton is hard, somewhat cork-like in consistency. Outer surface is covered with large, round calyces surrounded by a low, rounded ridge or lips. Its fleshy polyps have short, stout, rounded, tentacles in two rings. If the tentacles are retracted, the colony forms a dome-like lump. Oral discs are pushed against one another when fully expanded. Oral discs are up to 1.3 cm in diameter. Predators: Reef fish species (pomacentrid, Abudefduf saxatilis, monacanthid, Cantherhines macrocerus, and pomacanthids, Pomacanthus arcuatus and P. paru). Life cycle: Zoanthids may reproduce both sexually and asexually. Sexually by means of producing gametes, released for external fertilization as in hard corals. Asexual reproduction is by budding, where polyps divide to enlarge the colony. Envenomation, Deeds et al. (2011) and Blaxter et al. (1984) reported that the venom of this venomous species possessed haemolytic, anticancer and antigiardial activities. Further, a peptide isolated from this species caused a delay on the sodium current inactivation in voltage-gated sodium channels Nav1.7 of the superior cervical ganglion neurons of the rat. The palytoxin which is one of the deadliest toxins ever discovered in zoanthids is thought to be the most toxic, and it can kill or even paralyse humans in the minutest quantities especially when handled and there is break in the skin. It is believed however that the palytoxin is not produced by the zoanthids themselves but rather by a bacteria which may be present in the polyps and reside symbiotically (Anon. https://sta.uwi.edu/fst/lifesciences/sites/default/files/lifesciences/documents/ogatt/ Palythoa_caribaeorum%20-%20White%20Encrusting%20Zoanthid.pdf).

Palythoa heliodiscus (Ryland & Lancaster, 2003) (¼ Palythoa vestitus)

Image credit: Flickr Common name (s): Sunray zoanthid Global distribution: Hawaii and Indo-Paciﬁc. Ecology: It is occasional on shaded vertical surfaces in shallow water exposed to wave action and low light; at depths >5m. 264 6 Biology and Ecology of the Venomous Marine Anthozoans (Class Anthozoa)

Biology Description: Colonies of this species are stoloniferous and its large oral disk is with visible septae. Column is lacking stripes. Polyps are not always tightly packed; and they are brown with ﬁne lines radiating from the mouth. There are very short tentacles which are >60 in number. It attains a diameter of 2.5 cm. Envenomation: The venom of this species is highly toxic with palytoxin or palytoxin-like compounds (Deeds et al. 2011). Anon. (https://www.coralbiome.com/en/2011/11/21/palytoxine-danger/) reported that it contains the most potent non-protein compounds in dangerous quantities.

Palythoa mutuki (Haddon & Shackleton, 1891)

Image credit: Flickr Common name (s): Broad zoanthid Global distribution: Tropical Indo-Paciﬁc. Ecology: This sessile species is found on coral rubble and overhangs and among seagrasses in large seagrass meadows, with a depth range of 0–28 m. Biology Description: Colonies of this species are generally 5–10 cm. Its long body column raises the oral disk above the common tissue. Polyps are not embedded in a thick common tissue but are joined to one another at the base by underground stems (called stolons). Each polyp is about 1–2 cm in diameter with a wide oral disk on a long stout body column. Oral disk has furrows that radiate from the mouth to the edge of the disk. Sometimes with one white furrow so the disk appears to have one split. This zoanthid incorporates sand in its body, so its body column feels rough to touch. It has relatively short tapered tentacles. Body column is usually beige or brown and oral disk is brown or green. Life cycle: These zoanthids can multiply by budding. Envenomation: This species has been reported to contain the highly toxic palytoxin (Anon. http://www.wildsingapore.com/wildfacts/cnidaria/others/zoanthid/ mutuki.htm). 6.24 Family Sphenopidae 265

Deeds et al. (2011) reported that the venom of this species is weakly toxic but with haemolytic properties.

Palythoa toxica Walsh & Bowers, 1971

Image credit: Melissa Crimo and Nano-Reef.com Common name (s): Seaweed of death from Hana, deadly seaweed of Hana Global distribution: Tropical Pacific Ocean; it is native to Hawaii. Ecology: It is an a euryhaline species and is found in shallow pools (with freshwater inflows) of 25 cm deep; also grows across the rock surface. Biology Description: It is an encrusting species with a firm, tough cuticle. Polyps are partially embedded in a cushiony mat of coenenchyme which incorporates sand grains and fragments of debris. Oral disc of each polyp is broad and has a fringe of tentacles. Polyps can close up and they can be retracted into the coenenchyme, which then displays a pitted surface. Colour of this species is variable but is usually with some shade of cream, grey or pale brown. Envenomation: This species is equally toxic all year round. It has been suggested that its toxin is actually produced by a dinoflagellate, Ostreopsis spp., and is incorporated into the zoanthid tissues, possibly through a symbiotic relationship similar to that of zooxanthellae in coral (Anon. https://en.wikipedia.org/wiki/ Palythoa_toxica). Patocka et al. (2015) reported that its lethal palytoxin which ranks among the most potent of all marine toxins attacked all animal cells and caused a very wide spectrum of pharmacological effects. Initial symptoms which started 2 h after contact included shivering, myalgias and general weakness of the extremities, progressing to dizziness and speech disturbance at the time of collapse. Further, human illness and death which resulted from the consumption of crabs and fish contaminated or suspected to be contaminated with palytoxin have been reported in 266 6 Biology and Ecology of the Venomous Marine Anthozoans (Class Anthozoa) tropical and subtropical regions. Cases of death and near-death illness resulting from palytoxin have also been reported due to consumption of contaminated crabs in Philippines, sea urchins in Brazil and fish in Japan. Mariottini and Pane (2010) reported that the palytoxin which is a local anaesthetic and vasoconstrictive agent was also found shown to induce ion currents (channels permeable to Na+ and K+ and slightly permeable to Ca2+, choline and tetramethylammonium) in mouse neuroblastoma cells. The toxic effects of this species were known to the early inhabitants of Hawaii, and these zoanthids were applied to the tips of their weapons to become lethal (Anon. https://en.wikipedia.org/wiki/Palythoa_toxica).

Palythoa tuberculosa (Esper, 1805)

Image credit: Wikimedia Commons Common name (s): Sea mat zoanthids, brown sea mat zoanthids Global distribution: Indo-West Paciﬁc Ocean: Red Sea, Madagascar, Japan and Australia. Ecology: It inhabits reef slopes and also found in lagoons where they form encrusting mats of densely packed polyps at depths between 3 and 12 m. It is often found in areas where waves crash onto the rocks in shallow waters. Biology Description: Colony of this species is 20–40 cm tall. Each polyp is about 1–2cm in diameter and is embedded in a common tissue. Polyp has a thick and short body column, topped by a wide oral disk edged with tentacles in two rows. When the polyps are expanded, their oral disks and tentacles may hide the common tissue. Further, when the colony is out of water, tentacles and oral disks are tucked into the body column, leaving on small puckered holes on the surface of the common tissue. Colours of the colonies include brown, cream and yellow. 6.24 Family Sphenopidae 267

Envenomation: The toxic mucus of this species, on contact with eye, mouth or an open wound, can cause various disorders including numbness, hallucinations or even death (Goemans 2012b) These zoanthids contain the highly toxic palytoxin. It is reported that the Hawai- ian natives produced poisoned arrows by rubbing the tips on this zoanthid. It is believed that the toxins are not produced by the animal but by bacteria that live in symbiosis with the polyps (Anon. http://www.wildsingapore.com/wildfacts/ cnidaria/others/zoanthid/tuberculosa.htm). Suput (2011) reported that the lethal neurotoxin of this species viz. palytoxin caused sustained and TTX-insensitive depolarization of excitable membranes. This effect was followed by an inﬂux of Ca2+, which caused a wide variety of secondary actions such as cytoskeleton disruption and tumour promotion in the skin.

Palythoa vestitus (Verrill, 1928)

Common name (s): Not designated Global distribution: Hawaiian and other Paciﬁc Islands. No other information is available on the biology and ecology of this species. Envenomation: Wiles et al. (1974) and Blaxter et al. (1984) reported that the palytoxin of this venomous species produced marked irritant and tissue damage on contact to skin or eyes, as well as having a general necrotizing action on cells when injected. Anon. (http://www3.ufpe.br/gpa/images/documentos/ToxinasAnimais/primer% 20artigo%20de%20palitoxina.pdf) reported that the palytoxin of this species was found to be highly toxic/lethal in mice by intravenous injection. 268 6 Biology and Ecology of the Venomous Marine Anthozoans (Class Anthozoa)

6.25 Family Stichodactylidae

Heteractis aurora (Quoy & Gaimard, 1833) (¼ Radianthus koseirensis)

Image credit: Patrick Randall Common name (s): Beaded sea anemone, aurora host anemone, sand anemone, carpet anemone, flat anemone, corn anemone, Ritteri anemone, saddle tip anemone, adhesive sea anemone and white beaded anemone. Global distribution: Micronesia as well as in Melanesia to East Africa; Red Sea, and in Australia to the Ryukyu Islands. Ecology: This species lives among coral, and along rocky reef edges and on slopes, normally in areas with strong currents. It attaches to a surface and remains partially buried in sediment or sand. When threatened, it may retract entirely out of view into the substrate. Biology Description: Both the tentacles and oral disc of this species are brown or purplish. Its tentacles which reach 50 mm in length may be sticky when touched and can have tips of a magenta colouration. Longer tentacles contain swellings. These swellings appear on only on a single side, or almost entirely surrounding the tentacle, giving the appearance of beads on a string. A maximum of 20 such swellings may occur on any single tentacle. This species has a broad, flattened oral disc reaching 250 mm wide and may have white or brown markings that radiate from the centre, and they may even continue up and along the tentacles. Association: This anemone hosts seven species of anemonefish as symbionts. They are Amphiprion akindynos (barrier reef anemonefish), A. allardi (Allard’s anemonefish), A. bicinctus (two-band anemonefish), A. clarkii (Clark’s anemonefish), A. chrysogaster (Mauritian anemonefish), A. chrysopterus (orange- fin anemonefish) and A. tricinctus (three-band anemonefish). With seven species of 6.25 Family Stichodactylidae 269 hosted anemonefish, this species is a generalist anemone. However, it is considered a nursery anemone as, for reasons unknown, sexually mature fish are rarely hosted by this anemone species. Further, a number of other species are found associated with this anemone; however, this relationship is commensal rather than mutual as the anemone does not appear to benefit from the association. These species are porcelain crabs and shrimp of the genus Periclimenes. Envenomation: Nedosyko et al. (2014) reported that the crude venom of this species showed erythrocyte haemolysis, artemia lethality and shore crab neurotoxicity. Anderluh and Macek (2012) reported on the presence of cytolytic peptide and protein toxins (cytolysins) from this species.

Heteractis crispa (Hemprich & Ehrenberg, 1834) (¼ Radianthus macrodactylus; Radianthus crispus)

Image credit: Wikipedia Common name (s): Sebae anemone, leathery sea anemone, long tentacle anemone, purple tip anemone. Global distribution: Tropical and subtropical Indo-West Paciﬁc: from the eastern coasts of Africa, Red Sea included, to Polynesia and from south Japan to Australia and New Caledonia. Ecology: This reef-associated species is usually found subtidally among dead coral and rock rubble, from surface to 40 m deep. Biology Description: This anemone is characterized by a ﬂared oral disc which is 20–50 cm in diameter. It carries a number of tentacles (multiples of six), and they are 10–15 cm long and positioned in concentric circles. These tentacles are generally whitish, violet or greenish in colour, and tentacles of some specimens are found with beautiful blue, purple and mauve tips. Column is grey in colour and is dotted with sticky whitish “warts”. Usually this anemone has a grey or violet brown appearance overall, depending on the concentration of its symbiotic algae zooxanthellae. 270 6 Biology and Ecology of the Venomous Marine Anthozoans (Class Anthozoa)

Food and feeding: This anemone is a suspension feeder and it has two ways to feed. The first one is through the inside via photosynthesis of its symbiotic hosts zooxanthellae, living in its tissues. And the second one is through a normal way by capturing its preys via its tentacles that allow it to immobilize its prey which includes small invertebrates, fry or juvenile fish. Life cycle: Its reproduction can be sexual by simultaneous transmission of male and female gametes in the water or asexual by scissiparity. In the latter method, the anemone divides itself into two separate individuals from the foot or the mouth. Association: The anemone fish species hosted by this anemone are Amphiprion akindynos (barrier Reef anemonefish), A. barberi (barber’s anemonefish), A. bicinctus (two-band anemonefish), A. chrysopterus (orange-fin anemonefish), A. clarkii (Clark’s anemonefish), A. ephippium (red saddleback anemonefish), A. latezonatus (wide-band anemonefish), A. leucokranos (white-bonnet anemonefish), A. melanopus (red and black anemonefish), A. omanensis (Oman anemonefish), A. percula (clown anemonefish), A. perideraion (pink skunk anemonefish), A. polymnus (saddleback anemonefish), A. sandaracinos (orange anemonefish), A. thiellei and A. tricinctus (three-band anemonefish). Juveniles of Dascyllus trimaculatus are also found associated with this anemone species. Envenomation: This anemone uses its venomous cells or nematocysts found in their tentacles to sting (Anon. http://animal-world.com/Aquarium-Coral-Reefs/ Sebae-Anemone). Shiomi et al. (1997) reported that this species contains sodium channel toxin. Anderluh and Macek (2012) reported that this venomous species possesses cytolytic peptide and protein toxins (cytolysins). Frazão et al. (2012) reported on the presence of NaV channel toxins such as Rm1 to Rm5; Rc-1; Kv channel toxin, analgesic polypeptide HC1; Kunitz-type trypsin inhibitor IV; and cytolysins RTX-A and RTX-S-II. Tkacheva et al. (2011) reported on the presence of a new actinoporin Hct-S4 from this species.

Heteractis magniﬁca (Quoy & Gaimard, 1833) (¼ Radianthus magniﬁca; Radianthus paumotensis; Radianthus ritteri) 6.25 Family Stichodactylidae 271

Common name (s): Magnificent sea anemone, Ritteri anemone Global distribution: Throughout the tropical and subtropical Indo-Pacific: from the eastern coasts of Africa, Red Sea included, to Polynesia; and from south Japan to Australia and New Caledonia. Ecology: It favours hard substrates well exposed to light and current from the surface to 40 m deep. Biology Description: It is characterized by a flared oral disc which reaches between 20 and 100 cm in diameter. Oral disc, base of the tentacles and oral orifice have the same colour, from light beige to white. There are numerous tentacles which exceed 8 cm long and are in multiples of six and positioned in concentric circles. Their tips are fingered and often lighter in colouration than the tentacle body and are sometimes vividly coloured. Its name comes from the bright colour of the column, which is the visible outer structure. When the animal retracts, and these colours range from electric blue to green, red, pink, purple or brown. Food and feeding: There are two feeding methods. The first one is through the photosynthesis of its symbiotic zooxanthellae, living in its tissues, the second by capturing its prey with its tentacles that allow it to immobilize its prey which includes small invertebrates, fry or juvenile fish. Life cycle: The reproduction of this anemone can be sexual by simultaneous transmission of male and female gametes in the water or asexual by scissiparity, which means that the anemone divides itself into two individuals, separating from the foot or the mouth. Asexual reproduction is found only in the rim areas and is said to the origin of the large aggregations of this species in such areas. Association: The species of anemonefish hosted by this species of sea anemone include Amphiprion akallopisos (skunk anemone fish), A. akindynos (Barrier Reef anemonefish), A. bicinctus (two-band anemonefish), A. chrysogaster (Mauritian anemonefish), A. chrysopterus (orange-fin anemonefish), A. clarkii (Clark’s anemonefish), A. leucokranos (white-bonnet anemonefish), A. melanopus (red and black anemonefish), A. nigripes (Maldive anemonefish), A. ocellaris (false clown anemonefish), A. pacificus (Pacific anemonefish), A. percula (clown anemonefish) and A. perideraion (pink skunk anemonefish), H. magnifica also hosts Dascyllus trimaculatus, the three spot dascyllus and various commensal shrimps. Envenomation: Yamaguchi et al. (2010) reported on the presence of potassium channel toxin κ1.3-SHTX-Hm1a (HmK) from this species. 272 6 Biology and Ecology of the Venomous Marine Anthozoans (Class Anthozoa)

Anderluh and Macek (2012) reported on the presence of cytolytic peptide and protein toxins (cytolysins) from this species. Rodríguez et al. (2018), Frazão et al. (2012) and Shier (1990) reported on the presence of NaV channel toxins RpI, II, III and IV; Kv channel toxin HmK and cytolysins HMgI, HMgII and HMgIII from this species. Nedosyko et al. (2014) stated that the crude venom of this species showed erythrocyte haemolysis, artemia lethality and shore crab neurotoxicity. Ravindran et al. (2010) reported that the crude and partially puriﬁed venom of this species was cardiotoxic, nephrotoxic, hepatotoxic and neurotoxic to the internal organs of the mice. The associated chronic and lethal histopathological changes like haemolysis, thrombosis and myocardial haemorrhage in the heart; granulomatous lesions and damage to the hepatic cells in the liver; and haemorrhage throughout the kidney parenchyma and shrinkage of granular tufts in the kidney.

Heteractis malu (Haddon & Shackleton, 1893)

Image Credit: Wikimedia Commons Common name (s): Malu anemone, delicate sea anemone, white sand anemone Global distribution: From Japan in the north, to Australia in the south, east to the islands of Hawaii and west to Sumatra. Ecology: This is a lagoon anemone with a sand fetish. It favours ﬁne sand to burrow and lives, close to the surface. It remains buried in sediment up to the level of the oral disc. Biology Description: This anemone is quite decorative both in colour and appearance. It has short, stout and sparse tentacles which are under 40 mm in length and are usually tipped with magenta colouration. These tentacles vary in length, even among a single radial row. Its column has a pale cream or yellow colouration, with patches of deep yellow or orange sometimes present. Oral disc grows to a maximum diameter of 6.25 Family Stichodactylidae 273

200 mm and is brown or purplish, possibly with a white, radial pattern. It may sometimes be bright green, but this is rare. Association: The only anemoneﬁsh associated with this species is Clark’s anemoneﬁsh (Amphiprion clarkii). Envenomation: Nedosyko et al. (2014) reported that the crude venom of this species showed erythrocyte haemolysis, artemia lethality and shore crab neurotoxicity. Anon. (http://www.interhomeopathy.org/sea_anemone_must_protect_by_with drawal_inwardly) reported that this species possesses neurotoxic tentacles.

Stichodactyla gigantea (Forsskal, 1775) (¼ Stoichactis giganteus; Stichodactyla kenti)

Image credit: Michael arvedlund, Wikipedia Common name (s): Giant carpet anemone Global distribution: Indo-Pacific. Ecology: It resides on shallow seagrass beds or sand flats around 8 cm deep (at low tide); shores and usually on hard surfaces such as coral rubble, near reefs. Biology Description: This anemone has a maximum diameter of 80 cm. It can appear in a number of colours, commonly brown or greenish and rarely a striking purple or pink, deep blue or bright green. Its tentacles are extremely sticky to the touch, with firm adherence to surfaces. Its large oral disk expands when submerged and is covered with short tentacles so that it resembles a shaggy carpet. It is often folded and rarely held flat against the surface. Long body column is usually buried or inserted into a crevice and ends in a pedal disk that anchors the animal. Body column is sometimes colourful (bright pink, orange, yellow). Bumps (verrucae) appear as rows of spots, 274 6 Biology and Ecology of the Venomous Marine Anthozoans (Class Anthozoa) generally in bright colours (pink, purple). They are non-adhesive and are found on the upper part of the body column. Tentacles are short (about 1 cm), narrow and uniform in length. They are usually brown or purplish with lighter coloured tips. These tentacles are not very tightly packed and when submerged they are usually in constant motion; they are very sticky and may stick to a finger and break off. This anemone does not have a fringe of long-short tentacles at the edge of the oral disk. Food and feeding: This anemone harbours symbiotic single-celled algae (called zooxanthellae) which helps in its nutrition. Life cycle: There is not much information on how these anemones reproduce. Association: This species hosts seven different species of anemonefish, viz. Amphiprion akindynos (Barrier reef anemonefish), A. bicinctus (two-band anemonefish), A. clarkii (Clark’s anemonefish), A. ocellaris (false clownfish), A. percula (clownfish), A. perideraion (pink skunk anemonefish) and A. rubrocinctus (Australian anemonefish). This anemone is also the host of the juvenile Dascyllus trimaculatus. Envenomation: Carpet anemone has stingers in its tentacles. Generally, these stings do not hurt human beings, but they can leave welts on sensitive skin (Anon. http://www.wildsingapore.com/wildfacts/cnidaria/actiniaria/gigantea.htm). Hu et al. (2011) reported on the isolation of a new cytolysin gigantoxin-4 from this species. This toxin possessed a high haemolytic activity to human erythrocytes. Anderluh and Macek (2012) reported on the presence of cytolytic peptide and protein toxins (cytolysins) from this species. Frazão et al. (2012) stated on the isolation of NaV channel toxins gigantoxins 2,3; and ungrouped toxin gigantoxin-1 from this species.

Stichodactyla haddoni (Saville Kent, 1893) 6.25 Family Stichodactylidae 275

Image credit: Wikipedia Common name (s): Haddon’s sea anemone, saddle anemone Global distribution: Tropical and subtropical of Indo-Pacific: from Mauritius to Fiji and from the Ryukyu Islands of southern Japan to Australia. Ecology: It lives on sandy areas, among seagrasses and also on coral rubble. Biology Description: This anemone is characterized by a folded oral disc that reaches between 50 and 80 cm in diameter with a 1–2 cm tentacle-free oral area. Tentacles have a rounded tip and the end may be green, yellow, grey or rarely, blue and pink. Column has small, non-adhesive bumps (verrucae) which are usually the same colour as the column and not visible. Tentacles are yellowish or tan. At the circumference, this anemone has alternating short and long tentacles. This species can be coloured a bright green, reddish orange, grey, light green or even be striped. Its tentacles are so numerous on the surface of the oral disc, and it gives the anemone a “plush carpet” appearance (Brough and McBirney, 2015). Food and feeding: This anemone feeds in two ways. The first method is internal via photosynthesis of its symbiotic zooxanthellae, living in its tissues. And the second method is through capturing its prey like small invertebrates, fry or juvenile fish via its tentacles that allow it to immobilize its prey. Predators: Its predators include other anemones, nudibranchs, sea stars and some angelfish, triggers and large wrasses. Association: This species lives in association with six different species of clownfish, viz. Amphiprion akindynos (Barrier reef anemonefish), A. chrysogaster (Mauritian anemonefish), A. chrysopterus (orange-fin anemonefish), A. clarkii (Clark’s anemonefish), A. polymnus (saddleback anemonefish) and A. sebae (sebae anemonefish). Further, Juvenile Dascyllus trimaculatus also associates with this anemone. Furthermore, the porcelain crab Neopetrolisthes maculatus, shrimp Periclimenes sp. and the squat or sexy shrimp Thor amboinensis also live as commensals with this species of anemone. Envenomation: These anemones use their venomous cells or nematocysts found in their tentacles to sting. Generally, these stings do not hurt human beings, but they can leave welts on sensitive skin (Anon. http://www.wildsingapore.com/wildfacts/ cnidaria/actiniaria/haddoni.htm, http://animal-world.com/Aquarium-Coral-Reefs/ Saddle-Anemone). Toxins such as SHTX have been isolated from this species (Anon. https://en. wikipedia.org/wiki/Stichodactyla_haddoni). Yamaguchi et al. (2010) reported on the Kv1 potassium channel toxicity of this anemone species. Suput (2011) reported on anaphylaxis (severe allergic reaction) caused by a second contact. Ravindran et al. (2010) reported that the crude and partially purified venom of this species was cardiotoxic, nephrotoxic, hepatotoxic and neurotoxic to the internal organs of the mice. The associated chronic and lethal histopathological changes like haemolysis, thrombosis and myocardial haemorrhage in the heart; granulomatous 276 6 Biology and Ecology of the Venomous Marine Anthozoans (Class Anthozoa) lesions and damage to the hepatic cells in the liver; and haemorrhage throughout the kidney parenchyma and shrinkage of granular tufts in the kidney. Frazão et al. (2012) reported on the isolation of NaV channel toxins such as SHTX-4; Kv channel toxins SHTX-3 and SHTX-1/SHTX-2 and ungrouped toxin EGF-like peptide SHTX-5 from this species.

Stichodactyla helianthus (Ellis, 1768) (¼ Stoichactis helianthus)

Image credit: Wikipedia Common name (s): Sun anemone, Caribbean carpet anemone. Global distribution: Atlantic waters: common to occasional in Bahamas and eastern and southern Caribbean; and rare north-western Caribbean. Ecology: It is found along rocky shore lines in either large groups or a few individuals on rocks very near the surface in areas of surge, or on rocks and coral heads in sandy areas with little surge. It prefers shallow areas with mild to strong currents. Biology Description: It is a large, green, sessile, carpet-like sea anemone. It grows wide rather than tall and is covered with many short tentacles that make it look like a “plush” or “shaggy” carpet, thus the name. It has a ﬂattened oral disc covered with hundreds of short and thick tentacles which are with a rounded tip. Oral disc is up to 30 cm. Tentacles and oral disc are green to brown. This anemone has a sticky feel. Association: The anemone crab (Mithraculus cinctimanus) is often associated with this anemone. This crab is found among the tentacles or on the column and margin of the oral disc, as is the sun anemone shrimp. 6.25 Family Stichodactylidae 277

Envenomation: This anemone species excretes stichodactyla toxin (Anon. https:// en.wikipedia.org/wiki/Stichodactyla_helianthus). The venomous cells or nematocysts found in their sticky tentacles sting (Anon. http://animal-world.com/Aquarium-Coral-Reefs/Caribbean-Carpet-Anemone). Yamaguchi et al. (2010) reported on the presence of a potassium channel toxin κ1.3-SHTX-She1a (ShK) from this species. Shier (1990) reported on the occurrence of Sh-NI toxin from this species. Anon. (https://www.uniprot.org/uniprot/P81129) reported on the isolation of the toxin PI-stichotoxin-She2b from this species. Anderluh and Macek (2012) reported on the presence of cytolytic peptide and protein toxins (cytolysins) from this species. Frazão et al. (2012) reported on the presence of NaV channel toxin Sh1; Kv channel toxins SHPI-1, SHPI-2 and ShK; and cytolysins sticholysins I, II which are pore-forming toxins (PFTs) from this species.

Stichodactyla mertensii (Brandt, 1835)

Image credit: Wikipedia Common name (s): Mertens’ carpet sea anemone Global distribution: Tropical, Indo-West Pacific: East Africa, Malaysia, Indonesia, Japan and south to Australia and Fiji Islands. Ecology: This sessile species lives singly in rock crevices and on coral rubble on and near reef slopes and found at depths of 1–20 m. Biology Description: Diameter of this anemone is 1 m or more. Its large oral disk is covered with short tentacles so that it resembles a carpet. Oral disk is often held flat against the surface, unlike the Giant carpet anemone (Stichodactyla gigantea)in 278 6 Biology and Ecology of the Venomous Marine Anthozoans (Class Anthozoa) which the oral disk is often folded. Small pedal disc is frequently attached in crevice. This anemone can retract but not rapidly. Body column is tan to white with bumps (verrucae) that are adhesive and appear as rows of spots, generally in magenta or orange (which may appear purplish at depth). No verrucae are seen below wide upper column, but splotches of pigment continue down short, narrow column in more or less longitudinal streaks. Tentacles are not adhesive and are club-shaped to finger-like. All tentacles may be short (10–20 mm long), or some (in patches) very long (to 50 mm or more). Food and feeding: It contains obligate symbiotic zooxanthellae that help in its nutrition. Association: This anemone is host to around half the species of anemonefish and one damselfish, Dascyllus trimaculatus. The anemonefish which are hosted by this anemone include Amphiprion akallopisos, A. chrysopterus, A. leucokranos, A. clarkii, A. ocellaris, A. fuscocaudatus, A. sandaracinos, A. akindynos, A. Allardi, A. bicinctus, A. chrysogaster, A. latifasciatus, A. tricinctus, A. ephippium, A. polymnus and A. thiellei. Envenomation: Yamaguchi et al. (2010) reported on the presence of Kv1 potassium channel toxins from this species. The extracts of this species exhibited haemolytic effect on chicken, goat, cow and human erythrocytes. Further, its crude extract also showed neurotoxic effects and mortality of the sea shore crab Ocypode macrocera (Thangaraj and Bragadeeswaran 2012). Anderluh and Macek (2012) reported on the isolation of cytolytic peptide and protein toxins (cytolysins) from this species. Veeruraj et al. (2008) reported that the crude toxic protein (venom) of this species showed neurotoxic activity; and haemolytic activity on chicken, cow, goat and human erythrocytes.

Stichodactyla tapetum Hemprich & Ehrenberg, 1834 6.26 Family Thalassianthidae 279

Common name (s): Mini carpet anemone Global distribution: Red Sea, eastern coast of Africa; Indo-Pacific: southern Japan, south to Great Barrier Reef; Chek Jawa and Changi; Philippines, Vietnam. Ecology: It is found usually among seagrasses. Biology Description: This anemone which is green or tan has a maximum size of 15 cm. Oral disk is of 2–6 cm in diameter. Tentacles are very short and they look more like bumps. Tentacles are not so tightly packed together and especially in the centre and are neatly arranged into wedge-shaped groups, resembling the spokes of a wheel. Outer edge of the oral disk does not have a fringe of alternating long-short tentacles like Haddon’s carpet anemone (Stichodactyla haddoni). Food and feeding: Its ideal foods consist of small fish, shrimp and other meaty marine foods such as mysids and brine shrimp. Association: This anemone is not known to act as a host to clownfish species. However, anemone crabs and anemone shrimp are often observed on and around these anemones in the wild. Envenomation: Venomous; although this mini carpet anemone can sting like other anemones, it is not an aggressive anemone (Anon. https://www.liveaquaria. com/product/3219/?pcatid¼3219). Yamaguchi et al. (2010) reported on the Kv1 potassium channel toxicity of this species.

6.26 Family Thalassianthidae

Actineria villosa Quoy & Gaimard in de Blainville, 1830 Image not available Common name (s): Okinawan sea anemone Global distribution: Okinawa, Japan. Ecology: It occurs in coastal areas. Biology Description: Not reported Envenomation: Anon. (https://www.uniprot.org/uniprot/Q76DT2) reported on the presence of the toxin DELTA-thalatoxin-Avl2a from this species. Uechi et al. (2005) reported on the presence a haemolytic toxin from this species. Uechi et al. (2011) reported on the presence of a lethal protein toxin from this species. Oshiro et al. (2004) reported that this species caused severe cases of stinging which was attributed to its toxin designated as AvTX-60A. This toxin showed fatal toxicity to mice with intraperitoneal injection. Frazão et al. (2012) reported on the occurrence of toxins such as cytolysins Avt-I, Avt-II and AvTX-60A; and an ungrouped toxin Avt120 from this species. 280 6 Biology and Ecology of the Venomous Marine Anthozoans (Class Anthozoa)

Cryptodendrum adhaesivum (Klunzinger, 1877)

Image credit: Wikipedia Common name (s): Adhesive anemone, pizza anemone, nap-edged anemone Global distribution: Tropical Indo-West Pacific Ocean: Red Sea, Maldives, Thailand and north to Southern Japan and south to Australia. Ecology: These anemones are found in shallow waters of 1–7 m deep and in rock crevices or underneath stones where sand or coral gravel is piled up. Biology Description: This anemone grows to a size of 30 cm and is distinguished by its coloured, beaded and waving curved edge. It has two different forms of tentacles. At the centre of the oral disc, it has narrow, short, about 5 mm long, tentacles that are branched with five or more “fingers”, like a small, inflated rubber glove. These tentacles are extremely sticky. Tentacles at the edge have a bubble-like thickening of about 1 mm diameter at the end. These two types of tentacles are in different colours. Colours of these anemones range from blue and grey, pink and yellow, grey and purple and brown and green. Food and feeding: Like all symbiotic anemones it hosts zooxanthellae, symbiotic algae that help feed their host. This anemone is also a zooplankton feeder. Association: This anemone is associated with the juvenile Dascyllus trimaculatus, the three spot dascyllus. Further, a number of other species such as Neopetrolisthes maculatus, a porcelain crab; shrimp from the Periclimenes genus; and Thor amboinensis, the squat or sexy shrimp are also found associated with this anemone species. However, their relationship is commensal rather than mutual as the anemone does not appear to benefit from the association. Envenomation: Anon. (https://www.uniprot.org/uniprot/D2KX90) reported on the presence of Delta-thalatoxin-Cad1a from this species. Yamaguchi et al. (2010) reported on the Kv1 potassium channel toxicity of this species. 6.26 Family Thalassianthidae 281

Frazão et al. (2012) reported on the occurrence of NaV channel toxin Ca I from this species.

Heterodactyla hemprichii Ehrenberg, 1834

Image credit: Wikipedia Common name (s): Hemprich’s sea anemone Global distribution: Tropical, western Indian Ocean; Red Sea, Zanzibar, Sumatra, Emma Bay, Australia and India. Ecology: This species inhabits coral reef at 12 m depth where it may be found attached to coral. Biology Description: Fully expended anemones may reach 140 mm in diameter. Column is urn-shaped and upper part of column is with verrucae. Its whole oral disc is filled with tentacles which are closely arranged. Oral disc has permanent tentacular lobes which bear the cluster of nematospheres at the aboral face and the branched tentacles on the oral face of the tentacular structure. Exocoelic tentacles are orally and aborally flattened and endocoelic tentacles are short, branched and are radially arranged from the mouth to margin of oral disc. Mesenteries present at distally are more than the proximal part. Column is light coloured with purplish verrucae. Tentacles are green in colour and nematospheres are green with fluorescent yellow spots. Association: This anemone is found associated with some species of commensal anemone shrimp. Envenomation: Anon. (https://www.uniprot.org/uniprot/D2KX91) reported on the presence of toxin Delta-thalatoxin-Hhe1a from this species. Anon. (https://www.uniprot.org/uniprot/E2S065) reported on the presence of a toxin Kappa-thalatoxin-Hhe2a from this species. 282 6 Biology and Ecology of the Venomous Marine Anthozoans (Class Anthozoa)

Yamaguchi et al. (2010) reported on the Kv1 potassium channel toxicity of this species. Frazão et al. (2012) reported on the occurrence of a NaV channel toxin Hh x from this species.

Thalassianthus aster Ruppell & Leuckart, 1828

Image credit: Wikipedia Common name (s): Fuzzy-tipped anemone Global distribution: Tropical, north-west Paciﬁc, western Indian Ocean; Red Sea, Zanzibar and India. Ecology: It inhabits hard surfaces in reef rock areas including dead corals at a depth of 10 m, and it is completely buried in the layer of sand. It is even existing symbiotically on top of other motile invertebrates such as hermit crabs. Biology Description: Fully expended anemones of this species are with 40 mm in diameter. Upper part of column is with verrucae. Pedal disc is well-developed. Oral disc has permanent tentacular lobes which bear the grape-like nematospheres at the aboral face and the branched tentacles on the oral face of the tentacular structure. Marginal tentacles are orally and aborally ﬂattened and set at the margin not more than one exocoel. Mouth is round, and siphonoglyphs are not connected with directives. Mesenteries at the distal region of column are not more than the mesenteries at proximal part. Column is off white with light pink verrucae. Tentacles are purplish brown in colour and the nematospheres are olive green. Envenomation: Anon. (https://www.uniprot.org/uniprot/D2KX92) reported on the presence of Delta-thalatoxin-Tas1a from this very stinging species. The nematocysts of this species contain a Type-II Na+-channel toxin known as δ-TLTX-Ta1a (Anon. https://en.wikipedia.org/wiki/Thalassianthus_aster). 6.27 Family Xeniidae 283

Yamaguchi et al. (2010) reported on the Kv1 potassium channel toxicity of this species. Frazão et al. (2012) reported on the presence of a NaV channel toxin Ta I from this species.

6.27 Family Xeniidae

Heteroxenia fuscescens (Ehrenberg,1834)

Image credit: Wikipedia Common name (s): Pulsating xenid Global distribution: From Red Sea to Indian Ocean. Ecology: These corals live on hard bottoms of lagoons and bays, and slopes with little current. Biology Description: Polyps of this species grow to form large clumping colonies up to 60 cm across. Its polyp stalks are approximately 5 cm long and each stalk is ending in a ring of large feathery pinnate tentacles which are eight per polyp. Polyps pulsate rhythmically around 40 times/min, moving their tentacles in a “pumping” or “pulsating” fashion. This pulsing may create a current to assist feeding, respiration and helping to dispose of waste and detritus. It contains zooxanthellae and draws most of 284 6 Biology and Ecology of the Venomous Marine Anthozoans (Class Anthozoa) its energy from these symbionts. Two types of nematocysts viz. atrichous isorhiza- type of nematocysts and macrobasic-mastigophore nematocysts are seen in the tentacles of this species. Association: Symbiotic zooxanthellae. Envenomation: The venom of this species was found to be more haemolytic, more dermonecrotic and had more vasopermeable factors (Radwan et al. 2002). Partly isolated proteins (pro-inﬂammatory substances) from the nematocyst venom of this species have been reported to cause dermonecrosis and oedema when injected locally in sub-lethal concentrations (Suput 2011).

6.28 Family Zoanthidae

Zoanthus sociatus (Ellis & Solander, 1786)

Image credit: Jessica Rosenkrantz Common name (s): Green sea mat, button polyp Global distribution: Tropical: from Caribbean to south-eastern Brazil. Ecology: This sessile species lives in lower intertidal and upper subtidal zones (less than 30 m) on protected coral reefs and on disturbed substrate. It can survive desiccation (an excessive loss of moisture) and lower levels of salinity. Biology Description: This species exists as clonal colonies with crowded polyps. Each colony may reach a large size of 1.5 m2 without sand grain in the coenenchyme. Polyps are 3–30 mm high and 3–25 mm diameter. It is zooxanthellate. Food and feeding: Polyps of this species obtain nearly half of their required energy from their symbiotic zooxanthellae. It will eat mostly anything that is the right size such as from artemia cysts and dissolved organic matter. Life cycle: Reproduction in this species is mainly asexual although sexual reproduction may also happen. There is extratentacular budding, which is the creation of a new polyp from an old polyp, and ﬁssion. A colony is generally 6.28 Family Zoanthidae 285 genetically the same. Even when a colony is sexually reproductive, a large propor- tion of polyps remain infertile, which demonstrates the greater importance of asexual reproduction and growth. In sexual reproduction, colonies of this species do not become reproductive until they reach a certain size. They use external fertilization and are mostly hermaphroditic, although some are male or protogynous (female and then male). Association: Symbiodinium pilosum (dinoﬂagellate) Envenomation: The nematocyst venom of this species has been shown to be lethal to mice. Further, the same fraction was found to be a potential negative modulator of voltage-gated Ca2+ channels inhibiting the release of insulin in pancreatic β-cells (Lazcano-Pérez et al. 2016). Venomology of Marine Cnidarians 7

7.1 Venom Apparatus in Marine Cnidarians

Animals from the phylum Cnidaria are characterized by the presence of the cnidocyte, which is a combined sensory-effector cell that houses a subcellular ﬂuid-ﬁlled membranous organelle known as a cnida. Right combination of mechanical and chemical stimulation makes the cnidocytes evert the long tubular invagina- tion of its capsule wall explosively to the exterior. These cnidocytes are found aggregated in higher numbers on the tentacles, other prey-catching or defensive structures or near the mouth. There are three types of cnidae: penetrant nematocysts, volven spirocysts and glutinant ptychocysts, and they are housed in three types of cnidocytes: nematocytes, spirocytes and ptychocytes, respectively. All three types of cnidocytes can be found in sea anemones (Anon. https://www.gbri.org.au/ SpeciesList/Cryptodendrumadhaesivum%7CGuenHo.aspx?PageContentID¼4258; Mariscal et al. 1977). Nematocysts: Although nematocysts are mostly located on the tentacles, they also exist on the outer surface of the bell in certain species of the Alatinidae and Carybdeidae families, oral arms of Catostylus mosaicus (Schyphozoa) and the stomach (gastric cirri) of some cubozoans probably helping to paralyse and digest the prey. Aggregating anemones of the family Actiniidae have either specialized tentacles with nematocysts called acrorhagi or thread-like tissue containing nematocysts (located in the gastrovascular cavity of anemone) called acontia. While acrorhagi are used solely to deter other colonies from encroaching on their space, acontia serve as defense tissue against predators. Spirocysts: These organelles are present in most anthozoans and may differ morphologically among different taxonomic groups. The spirocyst capsule wall is thin and the everted tubule is helically folded. The tubule lacks spines but contains adhering, hydroscopic substances that mechanically immobilize the prey. Ptychocysts: These organelles have been reported in tube-dwelling members of Actinaria and Ceriantharia. They create the protective tube in which species from these families live.

# Springer Nature Singapore Pte Ltd. 2020 287 R. Santhanam, Biology and Ecology of Venomous Marine Cnidarians, https://doi.org/10.1007/978-981-15-1603-0_7 288 7 Venomology of Marine Cnidarians

Morphological properties of cnidae: The morphological properties of cnidae are taxonomically informative and help in distinguishing more distantly related species. For instance, the presence of spirocyst is characteristic of some anthozoans. In addition, the relative abundance of different types of nematocyst along with variation in the body size in several populations correlates to environmental factors, such as speciﬁc ecosystems, prey size and selectivity in prey capture. For example, Chironex ﬂeckeri has a relatively large body and a higher ratio of mastigophores (the longest of the penetrant cnidae) correlating to the large organisms which they prey upon.

7.1.1 Mechanism of Cnidae Discharge

The tentacles of the cnidarians contain from a few thousand to several billion nematocysts. These organelles are hollowed capsules containing a tightly coiled and folder thread immersed in the cnidarians’ venom. Nematocyst thread tubules evert so that the venom is injected on the outside of the thread tube. Some thread tubes are also hollowed and can discharge venom through the end. Nematocysts are discharged onto the skin within a fraction of a second, making a jellyfish nematocyst discharge one of the most rapid mechanical events in nature. Nematocysts can function even when separated or if the organism is dead although discharge rate decreases after death. The discharge of the jellyfish venom is triggered by mechanical stimuli (such as skin rubbing or tentacle traction), sudden increase in the osmotic pressure of the capsular fluid due to the removal of bound calcium ions and sudden relaxation of spring-like tensions in the nematocyst collagen framework. The above stimuli activate the uncoiling of the thread, which penetrates into the tissues, causing the nematocyst to discharge venom. Skin contact with jellyfish nematocysts resembles a prick, and the subsequent inflammation and nerve irritation produce pain, swelling and itching. These symptoms are potentially leading to skin necrosis in more severe stings (often from Australian chirodropid cubozoans). The local effect of the jellyfish venom is due to the penetration of the barbed threads or tubules of the nematocysts and the activity of various venom compounds like phospholipase A2 as well as exocytosis of mast cell granules (and, thus, possibly histamine release). These nematocysts can also cause potential systemic symptoms—as a result of the toxins entering the general circulation—including gastrointestinal (mainly Physalia physalis and Pelagiidae), muscular (Physalia and cubozoans), cardiac (Physalia and cubozoans), neurological (Physalia and cubozoans) and allergic manifestations (Pelagiidae and cubozoans). Jellyfish toxins reportedly also include haemolytic and lethal fractions. The lethal fractions of the jellyfish venom may also contain cardiotoxins which produce ventricular arrhythmias and cardiac arrest, and neurotoxins, which may cause respiratory failure and respiratory arrest. Intravascular haemolytic fractions of these jellyfish venoms can also precipitate acute renal failure. Cnidarians’ venom is also immunogenic, capable of generating antibody response (Cegolon et al. 2013). 7.2 Characteristics of Marine Cnidarian Venoms 289

7.1.2 Venom Apparatus in Sea Anemones

Sea anemones, like other cnidarians, possess numerous specialized stinging cells (cnidocytes) that are widely distributed throughout the body. These stinging cells are equipped with organelles known as nematocysts (cnidae), which contain small threads that are forcefully everted when stimulated. These nematocysts contain a complex cocktail of toxins that is used to envenomate predators and prey upon discharge. Nematocysts show significant variations in their density and morphology across different structures within sea anemones. For example, in Actinia tenebrosa, Actinia equina and Actinia fragacea, acrorhagi (wart-like spots used in aggressive intraspecific combat) contain holotrichs and basitrichs, while the tentacles (which are used in prey capture and defence) contain basitrichs and spirocysts; and basitrichs are also found in the mesenteric filaments, column, pedal disc and actinopharynx. The differences in cnidae composition are related to differences in the functional aspects of morphological structures, i.e. the capture of prey (crustaceans, small fish), defence against predators and intraspecific aggression (Prentis et al. 2018).

7.2 Characteristics of Marine Cnidarian Venoms

The venoms of marine cnidarians differ in composition, biological activity and potency among different species. Jellyfish venoms are complex and could be composed of potent proteinaceous cell membrane pores forming toxins, neurotoxic peptides, bioactive lipids, catecholamines, histamine, hyaluronidases, fibrolysins, kinins, phospholipases and various haemolytic, cardiotoxic, nephrotoxic, myotoxic and dermonecrotic toxins. Both the venom components and the tubule biopolymers can initiate different types of immunological responses—innate, adaptive, immediate or delayed hypersensitivity reactions—that can be amenable to anti-inflammatory 290 7 Venomology of Marine Cnidarians and immunomodulatory treatment. Thus, analysing each species-specific venom allows for appropriate and effective treatment (Lakkis et al. 2015). The diversity of venom components of marine and terrestrial animals ranges from non-proteinaceous compounds (e.g. purines, biogenic amines) to high-molecular- weight proteins. It is worthy of mention here that some toxin family types identified earlier in other venomous animals comprise the venom arsenal of cnidarians. For example Kunitz peptides which are presently found in sea anemones have already been identified in cone snails, insects, scorpions, spiders, reptiles, ticks and vampire bat. Further, the toxin, potassium channel blocker Kv1, evolved convergently in scorpions and sea anemones. Among the classes of the phylum Cnidaria, Anthozoa (sea anemones) has been paid some attention in regard to the venom. While many families of sea anemone peptide toxins have been described already, much still remains to be discovered about toxins in this group. It is interesting to note that only 236 peptide or protein toxins have been isolated from just 45 sea anemone species. This means that less than 4% (i.e. 45 species of more than 1100 species) of all sea anemones have had their venom peptides and proteins examined. It is further stated that the remaining 96% of species, particularly those distantly related to the super- family Actinioidea, may provide interesting new peptides with therapeutic potential. Some of the more venomous species, such as Telmatactis australiensis, Dofleinia armata and Triactis producta, should be especially interesting in this context (Prentis et al. 2018). The components of cnidarian venom exhibit striking diversity and include low-molecular-weight non-protein compounds such as serotonin and histamine, as well as high-molecular-weight complex proteins. This latter category includes enzymes, pore-forming toxins and neurotoxins targeting voltage-dependent ion channels. Of these, however, only enzymes (lipases and proteases) have been extensively characterized and firmly established as fundamental components of scyphozoan venom (Jouiaei et al. 2015; Remigante et al. 2018).

7.2.1 Enzymes

7.2.1.1 Phospholipase A2 Phospholipase A2 (PLA2) activity has been detected in the tentacles and acontia of anthozoans, schyphozoans, hydrozoans and cubozoans. This enzyme is commonly found in mammalian tissues where it plays important roles in dietary lipid catabo- lism, inﬂammation, etc. Further, it has also been found in reptiles (snakes and anguimorph lizard), centipedes, insects (their bristles, proboscises and stingers), arachnids (scorpions, spiders and ticks) and cephalopods. Toxic functions of PLA2 in cnidarian venoms include defence and immobilization and digestion of prey. Also, the PLA2 fraction of the acontial nematocysts of the sea anemone Aiptasia pallida has shown haemolytic activity.

7.2.1.2 Metalloproteases Metalloproteases are important venom components of terrestrial animals such as centipedes, snakes and ticks. These enzymes induce haemorrhage and necrosis by 7.2 Characteristics of Marine Cnidarian Venoms 291 preventing blood clot formation. These functions are commonly associated with the recurrent symptoms of cnidarian stings such as skin damage, oedema, blister formation, myonecrosis and inflammation. Metalloproteases were detected in the venom of jellyfish Stomolophus meleagris and Chironex fleckeri. Jellyfish metalloproteases have also shown proteolytic effects including gelatinolytic, caseinolytic and fibrinolytic activities. Zinc-dependent metalloproteases were detected in the nematocyst content of the sea anemone Nematostella vectensis.

7.2.2 Pore-Forming Toxins

The pore-forming toxins (PFTs) are present in all cnidarian venoms. These cause osmotic imbalance and cell lysis. Cnidarian PFTs are classiﬁed in two groups: α-PFTs and β-PFTs.

7.2.2.1 Actinoporins Actinoporins are α-PFTs and are present in anthozoa and hydrozoa. These basic proteins mediate various types of toxicity and bioactivity, such as cardiovascular and respiratory arrest in rats, lysis of chicken, goat, human and sheep erythrocytes and cytotoxic effects, all caused by a pore-forming mechanism.

7.2.2.2 Jellyfish Toxins (JFTs) Cubozoan-related porins are the most potent and rapid-acting toxins secreted by the different species of jellyfish. This toxin was first reported in the cubozoan Carybdea alata as CAH1, also reported as CaTX-A/B. Subsequently it was isolated in all cubozoans examined including CrTX-A/B from Carybdea rastoni, CqTX-A from Chiropsalmus quadrigatus and CfTX-1/2 and CfTX-A/B/Bt from Chironex fleckeri. Homologues of cubozoan porins were reported in Scyphozoa (Aurelia aurita), Hydrozoa (Hydra magnipapillata), Anthozoa (Aiptasia pallida) and various hydroids (Hydractinia symbiolongicarpus and Hydra vulgaris). Among CfTX toxins, CfTX-1/2 has been reported to cause cardiovascular collapse within 1 min in anaesthetized rats exposed in vivo to the venom, whereas CfTX-A/B was more potent in eliciting in vitro haemolytic activity.

7.2.2.3 Hydralysins-Related Toxins In addition to porins found in cnidarians, a novel β-PFT toxin has been isolated from the digestive endodermal cells of green hydra (Chlorohydra viridissima). These non-nematocyst, body-derived toxins play a role in lysing prey tissues.

7.2.2.4 Membrane Attack Complex–Perforin This group of β-PFT toxins have been detected in the venoms of the sea anemones, Phyllodiscus semoni and Actinaria villosa. These proteins have been reported to create a transmembrane pore into the target cell and initiate various apoptotic cell death pathways. 292 7 Venomology of Marine Cnidarians

7.2.3 Neurotoxins (Voltage-Gated Ion Channel Toxins)

Cnidarian neurotoxins are a group of peptides produced by sea anemones. These toxins help these sessile animals to immobilize the prey rapidly. They prolong the action potential of the excitable and non-excitable membranes in sensory neurons and cardiac and skeletal muscle cells via modifying the sodium channel gating or blocking the potassium channel. This causes the cell to become hyperactive and to release massive amounts of neurotransmitter at synapses and neuromuscular junctions that can cause initial spastic stage followed by descending ﬂaccid paralysis. Sea anemone voltage-gated ion channel toxins are the valuable bioresources to study the function of sodium and potassium channels and are of great pharmaceutical value as they may be used in the development of new drugs. Several cnidarian neurotoxin polypeptides have been reported to block Vanilloid Receptor 1 (transient receptor potential cation channel subfamily V member 1, TRPV1) and acid-sensing ion channel 3 (ASIC3), which take part in initiation and transduction of pain and hyper-algesia. These peptides are therefore promising tools for the development of novel pain reducers.

7.2.3.1 Voltage-Gated Sodium (Nav) Channel Toxins Voltage-gated sodium (Nav) channel toxins (NaTxs) of anthozoans bind to site 3 (loop S3–S4 in D4) of the Nav channels resulting in considerable neurotransmitter release in synapses. These NaTxs are divided into three groups: (i) type I NaTx; (ii) type II NaTxs and (iii) type III family which includes short peptides (~30 amino acids long). While the ﬁrst two types perform more or less similar functions, type III exhibit very high selectivity towards arthropod sodium channels.

7.2.3.2 Voltage-Gated Potassium (Kv) Channel Toxins and Kunitz Peptides Sea anemone voltage-gated potassium (Kv) channel toxins (KTxs) are categorized in ﬁve groups. Type I KTxs inhibit the potassium current through channels Kv1 and Kv3 subfamilies and intermediate conductance calcium-activated potassium channels. Type II KTxs are Kunitz peptides that have dual function of activity. Usually they act against trypsin and chymotrypsin proteinases in order to inhibit the rapid degradation of the venom protease by endogenous enzymes of the animals themselves. Several species of sea anemone Kunitz peptides possess both Kv-blocking activity and protease-inhibiting activity. For example, kalicludin 1–3 from the sea anemone A. sulcata binds competitively to Kv1.2 channels to paralyse the victim rapidly. Type III KTxs block a variety of distinct potassium ion channels such as Kv3.4 channel and hERG (the human Ether-à-go-go-related gene). Type IV are peptides from the sea anemone Stichodactyla haddoni that displays crab paralysis activity. Type V from the sea anemone Bunodosoma caissarum has been found to be active on Drosophila Shaker IR channels. 7.2 Characteristics of Marine Cnidarian Venoms 293

7.2.3.3 Small Cysteine-Rich Peptides (SCRiPs) These neurotoxins have been reported from the ectoderm of the coral Acropora millepora, and homologues of this toxin group have been isolated from the sea anemones Anemonia viridis and Metridium senile. The injection of these toxins (from A. Millepora) in zebraﬁsh (Danio rerio) larvae resulted in severe paralysis.

7.2.3.4 ASIC Inhibitors Sodium-selective acid-sensing ion channels (ASICs) have been associated with acidic pain during pathological conditions such as inﬂammation and ischaemia. The peptide π-AnmTX Ugr 9a-1 isolated from the venom of the sea anemone Urticina grebelnyi and another peptide PhcrTx1 from Phymanthus crucifer have been reported to target ASIC channels.

7.2.3.5 TRPV1 Inhibitors These neurotoxin inhibitors have been reported to initiate neuronal response during inﬂammation stimuli, which are one of the most important molecular triggers of pain stimuli. The ﬁrst peptide TRPV1 inhibitor viz. τ-SHTX-Hcr2b (APHC1) and two homologous peptides viz. τ-SHTX-Hcr2c (APHC2) and τ-SHTX-Hcr2d (APHC3) isolated from the venom of the sea anemone Heteractis crispa have been reported to be helpful in the designing a new generation of analgesic drugs.

7.2.4 Non-protein Bioactive Components

Apart from the protein and peptide compounds mentioned above, a number of pharmacologically active non-protein compounds have been detected in cnidarian venoms. For example, the non-protein toxin histamine has been isolated from the tentacles of the sea anemone species Anemonia viridis (¼ Anemonia sulcata) and Actinia equina. This compound produces sharp pain and increases vascular perme- ability. Although this compound has not been directly isolated from the nematocysts of the above species, it is likely that it is involved in cnidarian envenomation, and the present treatment with antihistamines for sting-associated symptoms supports this hypothesis. The non-protein toxin bunodosine isolated from the venom of the sea anemone Bunodosoma cangicum exhibits a potent analgesic activity. Further, caissarone isolated from the sea anemone Bunodosoma caissarum has a high antagonist activity towards guinea-pig ileum adenosine receptors. The detailed composition of sea anemone toxins is given below.

Composition of sea anemone toxins Protein type Structural family (i) Enzymes Endonuclease D, phospholipase type A2 (PLA2) and serine protease S1 (ii) Non-enzymatic Actinoporins, cysteine-rich proteins, cysteine-rich proteins proteins (CAP¼CRiSP), wall stress-responsive component (WSC) domain proteins (continued) 294 7 Venomology of Marine Cnidarians

(iii) Peptide Toxin (ATX-III), B-defensin-like, boundless β-hairpin, epidermal growth neurotoxins factor-like inhibitor cystine-knot, Kunitz-type protease inhibitors, proline-hinged asymmetric β-hairpin, small cysteine-rich peptides and ShK Source: Madio et al. (2019)

7.3 Envenomation of Marine Cnidarians

Among the different classes of the Cnidarian phylum, most health problems arise from the representatives of jellyfish, viz. the scyphozoans (true jellyfish), cubozoans (box jellyfish) and hydrozoans (siphonophores) (Montgomery et al. 2016). Jellyfish envenomation has become a serious health problem on coastal beaches throughout the world, but especially subtropical and tropical Atlantic, Pacific, Asian and Australian coasts where the most notorious jellyfish species prevail. It has been estimated that there are 150 million jellyfish stings a year, with some Pacific areas reporting up to 800 daily events at one single beach. Therefore, beyond being a public health issue, jellyfish also constitute a threat to tourism.

7.3.1 Venomous Species of Cnidaria

The most venomous cnidarian species of the different classes of this phylum are given below:

A. Hydrozoa (i) Medusae: Sarsia tubulosa, Pennaria disticha (¼ Pennaria tiarella) and Olindioides formosus (ii) Hydroids: Halecium beanii, Sertularia cupressina and Macrorhynchia philippina (¼ Lytocarpus philippinus), Millepora alcicornis (iii) Siphonophores: Physalia physalis B. Scyphozoa (i) Coronatae: Linuche unguiculata, Stephanoscyphus racemosus, and Nausithoe punctate (ii) Semaeostomae: Chrysaora colorata, Chrysaora hysoscella, Chrysaora quinquecirrha, Drymonema dalmatinum, Sanderia malayensis, Cyanea capillata, Cyanea lamarki and Pelagia noctiluca (iii) Rhizostomaea: Rhizostoma pulmo, Lobonema smithi, Cassiopea andromeda (¼Cassiopea xamachana), Acromitoides purpurus and Catostylus mosaicus C. Cubozoa (Box jellyﬁsh): Carybdea alata, Carybdea marsupialis, Carybdea rastonii, Tamoya gargantua, Chiropsalmus quadrigatus, Chironex ﬂeckeri and Tripedalia cystophora D. Anthozoa (i) Actiniaria (Sea anemones): Actinia equina, Sagartia elegans, Telmatactis decora (¼ Actinothoe longa), Adamsia palliata, Anemonia sulcata, Diadumene cincta, Corynactis australis, (continued) 7.3 Envenomation of Marine Cnidarians 295

Anthopleura elegantissima (¼ Bunodactis elegantissima), Anthopleura xanthogrammica and Rhodactis howesii (ii) Madreporaria (Stony corals): Acropora palmata Source: Russell (1965) and Montgomery et al. (2016)

7.3.2 Envenomation

Cnidarians (Coelenterates) contain thousands of specialized stinging cells (nematocysts) capable of penetrating the skin with harpoon-like threads and injecting venom upon contact. The potency of venom varies from species to species. The venom is composed of many protein fractions, some of which have been shown to be cardiotoxic, neurotoxic and dermatonecrotic. The venom may also contain histamine, prostaglandins, serotonin and kinin-like factors. Reactions are often instantaneous, but can be delayed. They usually consist of burning, itching and urticaria. Various types of skin lesions may develop after a sting, depending on the type of organism and the extent of the contact. Systemic manifestations are rare, except for the most toxic organisms. Anaphylaxis is becoming more common possibly due to the increasing number of people with previous contact, and sensiti- zation to coelenterate venom. There is a great diversity of cnidarian envenomations. At one end of the spectrum, there are serious envenomations, such as that of the box jellyfish Chironex fleckeri, which can kill a man in minutes; while at the other end, there are minor conditions such as an annoying itch. While the more serious or frequent envenomations are well-studied, others are rarely reported and poorly studied. Only a fraction of cnidarian toxins have been identified and thoroughly investigated. Rare cnidarian envenomations, such as fulminant hepatitis, autono- mous nervous system dysfunction or stroke, are not only interesting but also provide a wider perspective to cnidarian toxicology (Tezcan 2016). Maldonado et al. (2017) reported on the envenomation by a Physalia sp. in New Caledonia. Systemic envenomation by this marine hydrozoan included myalgia, rhabdomyolysis (increase in muscle enzymes) and acute renal failure. 296 7 Venomology of Marine Cnidarians

Rhabdomyolysis during envenomation by Physalia sp. (Images courtesy: Yann Barguil and Maldonado)

Skin lesions associated with Australian box jellyﬁsh stings. (Images credit: Professor Bart Currie, Menzies School of Health Research, Darwin, Australia) 7.3 Envenomation of Marine Cnidarians 297

Scar of Pelagia noctiluca injury. (Image Courtesy: Enis Karazincir)

An erythematous plague on the left forearm due to Chrysaora lactea. (Image courtesy: Vidal Haddad Junior)

7.3.3 Main Stinging Cnidarians

Species Local symptoms Systemic symptoms P. physalis Acute pain, wheals skin Muscular spasms, abdominal pain, arrhythmias, necrosis headache, D C. ﬂeckeri Pain, massive wheals, Severe hypotension, cardiac failure/arrest, vesicles, scarring arrhythmias, pulmonary hypertension, D C. quadrigatus Pain, wheals, swelling Asystole, bradycardia, hypotension, pulmonary hypertension/oedema, D (continued) 298 7 Venomology of Marine Cnidarians

C. quadrumanus Pain, wheals; scarring Hypotension, acute cardiac failure, pulmonary and dyschromia hypertension/oedema, D Carukia barnesi Muscular cramping Irukandji syndrome, hypertension, pulmonary pains oedema and heart failure D Morbakka Wheals, pain, itching, Irukandji syndrome (muscle spasms, back pain, vesicles, skin necrosis anxiety, respiratory distress, hypotension, sweating) C. rastoni Pain, wheals, swelling, No blisters C. alata Pain, wheals, blisters, Mild Irukandji syndrome, possible allergic dyschromia reactions Tamoya Burning pain, wheals, Muscle cramps, nausea, vomiting, restless, haplonema blisters/scarring sweating, headache Tamoya sp. Skin pain Mild to severe Irukandji syndrome P. noctiluca Instant severe pain, (Rare) allergic reaction and respiratory distress wheals C. quinquecirrha Intense pain, wheals/ (Rare) allergic reaction and respiratory distress, rash D C. capillata Pain, wheals, erythema (Possible) muscle cramps, sweating, nausea, allergic reaction Sanderia Skin pain, skin necrosis Peripheral vasospasm and tissue necrosis malayensis Carybdea sp. Skin pain Mild to severe Irukandji syndrome Gonionemus Joint, chest and loin Respiratory syndrome—allergic rhinitis, vertens muscle pains lachrymation, hoarseness, cough and dyspnoea Stomolophus Severe skin pain Sweating, nausea, vomiting, anxiety and nomurai restlessness, pulmonary oedema D D Deadly Source: Cegolon et al. (2013)

7.3.4 Jellyfish Envenomation and Irukandji Syndrome

7.3.4.1 Species Relating to Irukandji Syndrome The stings of jellyfish belonging to Hydrozoa (Physalia), Scyphhozoa (True jellyfish) and Cubozoa (Box jellyfish) have been reported to be responsible for the jellyfish envenomation-associated Irukandji syndrome. The species responsible for this syndrome are listed below

1. Carukia barnesii 2. Carukia shinju 3. Gerongia riﬁkinae 4. Alatina mordens. 5. Alatina rainensis 6. Malo maxima 7. Malo kingi 8. Carybdea alata 7.3 Envenomation of Marine Cnidarians 299

9. Carybdea xaymacana 10. Cyanea spp. 11. Physalia physalis 12. Gonionemus ohoro 13. Rhizostoma spp.

7.3.4.2 Symptoms of Irukandji Syndrome Patients

1. Local symptoms (a) The local symptoms associated with the Irukandji syndrome as identified in different case studies are given below (b) Sting area sweats profusely first and then entire body sweating (c) Profuse sweating and then non-sweating at the sting site which may be from initial anhydrosis followed by the compensatory hyperhydrosis (d) Tremor (e) Erythema or welts; diaphoresis or flushing (f) Moderate to severe pain (g) Minimal rash at sting site with slight redness and raised vesicles (h) Small insignificant puncture (i) Absence of wheals 2. Musculo-skeletal symptoms (a) Violent muscle cramps and muscle pain (b) Jaw pain (c) Joint pain (d) Cramping and spasms of intercostals and diaphragm (e) Chest pain (f) Severe pain the sacral or lower back area (g) Limp pain and abdominal pain (h) Hyperactive deep fluxes 3. Gastrointestinal symptoms (a) Nausea and vomiting (b) Pain in epigastrium 4. Neurological symptoms (a) Distress and anxiety (b) Severe frontal or global headache (c) Hypertension (d) Global cardiac dilation (e) Intraventricular tachycardia, and transient dilated cardiomyopathy (f) Irregular heart beats (g) Myocardial infarction (h) Cardiogenic shock 5. Miscellaneous symptoms (a) Oliguria (b) Priapism, allergic reactions (c) Respiratory distress (d) Uncontrolled tremor, hyperventilation 300 7 Venomology of Marine Cnidarians

(e) Dry mouth, burning eyes, sharp pickling sensation, cold, violent shivering, cough (f) Squirting redness (g) High temperature, pyrexia (h) Shock, collapse (i) High stimulation of sympathetic system (j) Periorbital oedema (k) Pulmonary oedema

Globally recorded Irukandji syndrome stings. (Source: Carett et al. 2012)

7.3.5 Sea Anemone Envenomation

Sea anemones are widely distributed, and all swimmers are at risk of contact. Contact with anemone tentacles may cause light burning, redness or transient wheals. Some species in the Caribbean, east Atlantic and Mediterranean cause more painful, severe stings. Dangerous species are mostly found in a range of habitats in the Indo-Pacific region, including the Red Sea. They cause severe local reactions and sometimes generalized symptoms; rarely, they can cause death (Anon. file:///C:/Users/santhanam/Downloads/marine-hazards-traveler-summary.pdf). Among the sea anemones, Actinodendron plumosum, Phyllodiscus semoni, Stichodactyla haddoni, Anemonia sulcata and Condylactis sp. have been reported to cause envenomation (Mizuno 2018). Unlike jellyfish stings, sting-associated injuries caused by sea anemones are relatively infrequent because most are fixed on or near the seafloor and generally do not move by themselves. Although most sea anemone toxins are only mildly harmful to humans, causing injuries such as 7.3 Envenomation of Marine Cnidarians 301 mild to moderate dermatitis, there are reports of envenomation by some species having extremely toxic effects in humans, including severe swelling and necrotizing dermatitis accompanied with skin ulceration, and some cases have even been accompanied with systemic reactions such as systemic shock syndrome, hepatic failure and acute kidney injury (AKI). Reports of envenomation by sea anemones causing AKI in humans are rare. However, the envenomation of sea anemones can induce AKI through direct toxic effects, abnormal haemodynamics, allergic reactions, haemolysis and rhabdomyolysis. Among the sea anemone species, Phyllodiscus semoni and Actineria (A.) villosa are highly toxic, and they are largely responsible for AKI in Japan (Mizuno 2018). Mizuno et al. (2000) also reported that the sea anemone sting victims of Sulu Sea around Cebu Island showed symptoms of severe swelling and pain in right arm, acute tubular necrosis and acute renal failure. Mizuno et al. (2012) in this report stated that the venom of Phyllodiscus semoni induced acute glomerular endothelial injuries in rats resembling haemolytic uremic syndrome (HUS), accompanied with complement dysregulation in glomeruli and suggested that the model might be useful for analyses of pathology and development of therapeutic approaches in HUS.

7.3.6 Globally Recorded Jellyfish Stings

Jellyﬁsh stings are common worldwide with an estimated 150 million cases annually (Al-Rubiay et al. 2009).

7.3.6.1 Brazil Forty-nine accidents caused by jellyfish (Cnidaria) were observed during a period of 5 years on the south-eastern coast of Brazil. The injured areas of the victims were mainly the legs (71%) and the trunk (65%). Twenty accidents were due to Chiropsalmus quadrumanus, 4 with Physalia physalis and 20 with unidentified jellyfish. All these victims had intense pain, linear plaques and systemic symptoms. The remaining five cases were largely due to Olindias sambaquiensis which caused mild pain, round plaques and no systemic symptoms. There are a few reports on accidents caused by jellyfish, in this country, and scarce clinical or epidemiological data are available up to the present moment (Haddad et al. 2002).

Jellyﬁsh associated with the injuries and clinical aspects observed in the patients Linear Round Systemic Accidents Paina plaques plaques symptomsb C. quadrumanus 08 ++ + À 08 C. quadrumanus 12 ++ + À 12 P. physalis 04 ++ + À 04 O. sambaquiensis 05 + À +2 Source: Haddad et al. (2002) a(+, mild; ++, intense) bNausea, vomiting, respiratory distress, malaise 302 7 Venomology of Marine Cnidarians

7.3.6.2 Hawai’ii In a period of 5 years, this country recorded 113 patients with cnidarian stings in western O’ahu, Hawai’i. The most common clinical feature of these victims was acute local pain, but cases of anaphylaxis or anaphylactoid syndrome and a persistent or delayed local cutaneous syndrome were also documented. Six cases resem- bled the Irukandji syndrome which was associated with severe pain and signs of catecholamine excess, including muscle cramping, elevated blood pressure, diaphoresis, and tremor.

Cnidarian envenomation syndromes at Wai‘anae, Hawai’I(n ¼ 113) Presentation signs and symptoms Number of cases Local pain and/or itching 59 Local pain with regional neurological symptom 3 Anaphylaxis/anaphylactoid syndrome 11 Irukandji-like syndrome 6 Mild systemic symptoms 7 Persistent/delayed cutaneous syndrome 21 Other 2 Unclassiﬁable 4 Source: Yoshimoto and Yanagihara (2002)

7.3.6.3 Queensland, Australia Anon. (https://www.weforum.org/agenda/2019/01/how-an-explosion-of-jellyﬁsh- is-wreaking-havoc/) reported that the bluebottle jellyﬁsh (Physalia physalis) was responsible for about 13,000 stings. This also leads to the closure of popular swimming spots.

7.3.6.4 Florida Anon. (https://www.weforum.org/agenda/2019/01/how-an-explosion-of-jellyfish- is-wreaking-havoc/) reported that over 1000 people were stung in Volusia County, Florida, following a period of exceptionally prolific jellyfish blooms. The explosion in their numbers has been attributed to warming seas and even increased pollution. Inman (2018) reported that jellyfish blooms stung more than 1000 people on a Florida beach. Anon. (https://www.usatoday.com/story/news/nation-now/2018/06/ 12/600-jellyfish-stings-florida/694679002/) reported that the Florida lifeguards treated more than 800 for jellyfish stings.

7.3.6.5 Scotland and Sweden Anon. (https://www.weforum.org/agenda/2019/01/how-an-explosion-of-jellyfish- is-wreaking-havoc/) reported that the reactors at the Torness nuclear power plant in Scotland were shut down after an invasion of jellyfish started blocking the cooling filters. In Sweden, the jellyfish blooms forced the closure of the Oskarshamn nuclear power plant, which contains the world’s largest boiling-water reactor. 7.3 Envenomation of Marine Cnidarians 303

7.3.6.6 Philippines Anon. (https://www.weforum.org/agenda/2019/01/how-an-explosion-of-jellyﬁsh- is-wreaking-havoc/) reported that the island of Luzon, home of the Philippines’ capital Manila, suffered a blackout in 1999 due to jellyﬁsh.

7.3.6.7 China (East Coast) Fenner (https://www.ilsf.org/sites/ilsf.org/files/filefield/treatmentofmarinestings. pdf) reported that the non-box jellyfish Stomolophus nomurai was responsible for human fatalities.

7.3.6.8 United States of America Fenner (https://www.ilsf.org/sites/ilsf.org/files/filefield/treatmentofmarinestings. pdf) reported that the non-box jellyfish Physalia physalis was responsible for human fatalities.

7.3.6.9 Australia, Brunei, Borneo, Indonesia (Kalimantan), Japan, Labuan, Malaysia (Penang and Langkawi Is.), Papua New Guinea, Philippines, Sabah, Sarawak, Solomon (Bougainvillea) Is., Kalimatan, Papua New Guinea, United States of America Fenner (https://www.ilsf.org/sites/ilsf.org/files/filefield/treatmentofmarinestings.pdf) reported that the box jellyfish caused human fatalities in these countries due to chirodropid envenomation. Fenner (2005) reported on the locations of deaths from cnidarians envenomation around the world as follows.

Locations of deaths from cnidarians envenomation around the world Jellyﬁsh Countries with fatalities Chirodropids (Box jellyﬁsh) Australia Brunei Indonesia (Kalimantan), Labuan Malaysia (Penang and Langkawi Is.) Japan (Okinawa) Papua New Guinea Philippines, Sabah, Sarawak Solomon Islands (Bougainvillea) Thailand, USA Carukia barnesii (Irukandji) Australia (North Queensland) Stomolophus nomurai China (around Qingdao—eight deaths) Physalia physalis USA (South-east—three deaths) Source: Fenner (2005) 304 7 Venomology of Marine Cnidarians

Globally recorded cnidarian envenomations. (Source: Tezcan 2016)

7.4 Treatment and Management of Marine Cnidarian Envenomations

Contact with a venomous cnidarian is often the discharge of thousands of vesicles leading to more or less serious clinical symptoms. In the majority of cases, the clinic consists of pain followed by minor local tissue damage, but injuries can be serious or life-threatening depending on the affected area or dangerousness of the venom of the concerned species. However, the first danger comes from paralysis secondary to deep pain with a risk of drowning. The second danger comes from the risk of anaphylactic reaction if the envenomed individual is already sensitized by a previous contact. It has been reported that immediately after the cnidarian envenomation on human, physical attempts to detach remaining tentacles from the victim’s skin may cause massive discharge. Since 1908, numerous traditional remedies such as urea, seawater, vinegar and methylated spirits have been used to inactivate the undischarged nematocysts on the adhered tentacles and/or to reduce pain. These chemicals lead to varying degrees of success, ranging from complete success in certain species to complete failure in others. For instance, while certain chemicals such as ethanol or 5% acetic acid in distilled water cause massive nematocyst discharge in Hydrozoa and Cubozoa species, some other such as a food-grade vinegar was found to inactivate the penetrating nematocysts of the box jellyfish Chironex fleckeri rapidly and completely. It therefore calls for a collaborative effort of medical, pharmacological, toxicological and biological disciplines towards effective therapeutics to minimize the pathogenic impact of venomous cnidarians on beach visitors, bathers and divers. 7.4 Treatment and Management of Marine Cnidarian Envenomations 305

7.4.1 Treatment and Management of Scyphozoan Stings (Remigante et al. 2018)

7.4.1.1 First-Aid Measures for Scyphozoan Stings Common sense dictates that prevention of jellyfish stings rather than treatment would be the better option. Beach closures and suspension of aquatic events in the case of jellyfish swarms, on-site protective nets in the water and warning signs on beaches would constitute some of the first-aid measures for the scyphozoan stings. These measures have been applied at least partly for Cyanea capillata and Pelagia noctiluca among Scyphozoa, and have also been put in place in Australia for the more dangerous cubozoans, including the deadly Chironex fleckeri and are advisable elsewhere. In case of scyphozoan stings, management first necessitates rescue and prevention of drowning and close monitoring of systemic reactions, especially anaphylaxis, which would require basic and advanced life support measures. If this is not the case, first-aid measures can be initiated with the aim of (i) preventing further discharge of nematocysts and (ii) limiting the action of the venom in terms of pain and tissue damage.

Prevention of Further Discharge of Nematocysts After a Sting Preventing further nematocyst discharge after a scyphozoan sting would limit the venom load and implies (i) removal of the tentacles and (ii) inactivation of nematocysts that may be adhering to the skin. Tentacle removal from the skin of the victim is necessary as detached tentacles are still capable of envenomation. Tentacle removal is a critical step as the procedure may trigger further nematocyst discharge. At best, tentacles should be removed with tweezers or similar tools as using bare hands may cause injury to the rescuer. Scraping of the sting site with various objects, such as a credit card or a razor, would be deleterious. As the application of pressure during this procedure may produce further nematocyst discharge, it is likely that it should also be avoided. For the same reason, pressure- inducing bandages (PIB) are no longer recommended.

Rinsing with Seawater Tentacle removal can also be attempted by thoroughly washing the area with an aqueous solution. The optimal washing medium should rinse off tentacles while inactivating nematocysts. Rinsing the sting site with seawater was found to help in tentacle removal, relief of pain and inhibition of venom discharge and is generally recommended in the case of Cyanea capillata stings and for Aurelia aurita, Nemopilema nomurai, and Pelagia noctiluca stings. However, the use of sea water for this purpose has to be conﬁrmed with further intensive studies.

Rinsing with Vinegar or Acetic Acid Vinegar has been found to signiﬁcantly decrease venom functional activity in Cyanea capillata. Similarly, 5% acetic acid did not induce nematocyst discharge per se and dramatically impaired discharge induced by a combined physico-chemical stimulation of oral arms of Pelagia noctiluca. 306 7 Venomology of Marine Cnidarians

Rinsing with Deionized, Distilled or Fresh Water There is no evidence in favour of the use of plain water at ambient temperature for scyphozoan stings.

Rinsing with Urine or Solutions Containing Urea or Ammonia Concerning Scyphozoa, urine, urea and ammonia were found to be either detrimental or ineffective with the notable exception of Pelagia noctiluca where ammonia was found to inhibit the in situ chemosensitizer-induced nematocyst discharge. Further, ammonia continues to be used as the main (74%) non-pharmacological treatment for jellyfish stings along the south Italian coast where most stings (61.81%) are attributed to P. noctiluca. The assessment whether ammonia can be used safely and efficaciously in the first treatment of patients with P. noctiluca stings is worth further investigation.

Additional Rinsing Solutions Among the various rinsing solutions that were assayed (acetone, alcohols including 70% ethanol and methylated spirits, and alkaline solutions), only methylated spirits were found to be of some beneﬁt for scyphozoan stings. Again, while generally found to be detrimental, 70% ethanol inhibited the in situ chemosensitizer-induced nematocyst discharge in Pelagia noctiluca. Stingose, an aqueous solution of 20% aluminium sulphate and 1.1% surfactant, was found to be of some use for Chrysaora quinquecirrha and Cyanea capillata stings as it inhibited nematocyst discharge. Commercially available proprietary formulations, such as the newly developed Sting No More® Spray (contents include vinegar, copper gluconate, urea and magnesium sulphate), was also found to reduce the venom load in an ex vivo model of envenomation from the scyphozoan Cyanea capillata and may work well for other scyphozoan stings.

Bicarbonate and Baking Soda Slurry Baking soda slurry was found to be of potential benefit for Chrysaora quinquecirrha and Cyanea capillata stings. However, there is no consensus for Pelagia noctiluca. Further studies are needed to confirm species-specific differences in the efficacy of this agent.

7.4.1.2 Limiting the Action of the Venom in Pain and Tissue Damage At present, there is no consensus on the action that should follow tentacle removal from the stung epidermis. The main objectives at this stage are to attenuate local pain and inﬂammation while preventing tissue damage, inactivating venom toxins and preventing venom diffusion and discharge of unﬁred nematocysts that can still adhere to the epidermis.

Heat or Cold Packs Cold packs, ice or immersion in cold water would limit inflammation and diffusion of the venom and relieve pain in jellyfish stings. While hot water immersion induced clinically significant pain relief, no statistically significant differences between hot 7.4 Treatment and Management of Marine Cnidarian Envenomations 307 water immersion and hot packs were found for the dermatological outcomes. A 45 C water immersion of the stung part for 20 min was found to be the best treatment. Heat was also unequivocally found to be beneficial for Aurelia aurita, Rhopilema nomadica and Stomolophus meleagris stings. On the other hand, for both Cyanea capillata and Pelagia noctiluca, both cold and hot packs have been found to be of benefit in different studies. Specifically, ice pack application was found useful in relieving the pain of stings from both species. However, in some studies, it was found that heat inhibited the Cyanea capillata venom activity while cold exposure was ineffective. It is also recommended that a 45 C water immersion for 40 min could be the best treatment for Cyanea capillata stings.

Lidocaine and Local Anaesthetics Topical lidocaine and hot water have also been found to reduce pain. Local anaesthetics were found to decrease skin redness and relieve pain after Chrysaora quinquecirrha stings. Immediate pain relief was obtained with 10% and 15% lidocaine solutions, but it took approximately 1 min to get the same effect with 4– 5% concentrations (Cegolon et al. 2013). Further, an inhibition of in situ chemosensitizer-induced nematocyst discharge was reported with 1% lidocaine in Pelagia noctiluca. At present, there is little evidence against the use of lidocaine although it may be a rarely available agent. Controlled clinical trials are warranted to unequivocally assess safety and efﬁcacy of the use of lidocaine and other topical anaesthetics after scyphozoan stings.

7.4.2 Treatment of Cubozoan Envenomation

7.4.2.1 First-Aid Treatment of Chirodropid (Cubozoans) Envenomation (Fenner https://www.ilsf.org/sites/ilsf.org/files/filefield/ treatmentofmarinestings.pdf)

1. The victim should be ﬁrst retrieved from the water, and is restrained, if necessary. 2. If helpers are available, victims may be sent immediately for ambulance/medical help (emphasize that the sting is from a Box jellyﬁsh as the ambulance may have antivenom available). 3. Victim’s airway, breathing and circulation (ABC) has to be assessed. He may be treated with mouth-to-mouth resuscitation (EAR), or heart massage (CPR), if necessary. 4. If resuscitation is not needed, vinegar may be poured over the stung area for a minimum of 30 s to inactivate remaining stinging cells on any adherent tentacles left on the skin. 5. After vinegar application, compression bandages may be applied directly over major stings. 6. If available, Chironex antivenom may be used for all major cases. Three ampoules each containing 20,000 units may be given intramuscularly, above 308 7 Venomology of Marine Cnidarians

the bandages, if there is a trained health professional on the beach. Medical personnel may give one ampoule intravenously. 7. Cold packs may be used (15 min and repeated when necessary) to help ease the skin pain in conscious victims. 8. In severe envenomation, oxygen may be used if available to assist with any breathing difﬁculty. Inhaled analgesia (i.e. entonox or penthrane) can be administered for unremitting pain in conscious, breathing, cooperative patients, and its use should be discontinued if the patient’s condition worsens.

7.4.2.2 Management and Treatment of Important Species of Venomous Cubozoans

Carybdea Alata In the case of Carybdea alata envenomation, it is first necessary to calm the victim and prevent him from rubbing to avoid over-envenoming. Visible tentacles have to be removed gently with heavy forceps or gloves. The little or no visible debris will be trapped in shaving foam, talc or dry sand and are removed by scraping the skin using a blue card for example. An abundant rinsing will then be done (at least 20 min) with seawater, or better, vinegar, which allows the inactivation of cnidocysts. The immersion of the party reached in hot water (50 C) has shown efficacy against the reduction of pain following a bite of this species. Then, the wound will be disinfected with an antiseptic (chlorhexidine) and then pain will be treated with analgesic (paracetamol Æ codeine). The use of opioids in accidents involving cubomeduses is sometimes necessary. If there is itching, corticosteroids and antihistamines will be used. The most severe accidents with open wounds or inflamed appearance may require the use of antibiotics and the injection of anti- tetanus serum, after verification of the vaccine status of the victim. The main goal of management of cubomeduse envenomation is the control of pain and blood pressure. Since there may be delayed hypotension to envenomation, primary hypertension should be treated with short-acting hypotensive agents and rapid elimination. Moni- toring of cardiac function with ECG should be performed in persons at risk (elderly, persons with cardiac history or under medical treatment). An elevation of troponins, a marker of myocardial pain, has been observed in victims whose pain is continuous despite the administration of opioid analgesics. In these people, a dosage can be made to ensure the health of the myocardium. In all cases, first aid should never delay cardiopulmonary resuscitation and hospital transfer in cases of severe envenomation or anaphylactic shock (Fenner https://www.ilsf.org/sites/ilsf.org/files/ filefield/treatmentofmarinestings.pdf).

Chironex Fleckeri (Fenner https://www.ilsf.org/sites/ilsf.org/files/filefield/ treatmentofmarinestings.pdf)

1. An ice pack may be applied and simple oral analgesia such as paracetamol may be given. 7.4 Treatment and Management of Marine Cnidarian Envenomations 309

2. Generous volumes of vinegar (acetic acid) may be applied to all visible sting sites to inactivate all the undischarged nematocysts (sting cells). 3. Titrated morphine (0.1 mg/kg IV up to 5 mg every 10 min) may be given to patients with pain refractory to ﬁrst-aid.

Reese and Depenbrock (2014) reported the following treatment options for Chironex ﬂeckeri and Carukia barnesii. Chironex ﬂeckeri: For local (cutaneous) symptoms such as painful purple linear plaques, oedema and erythema, hot water immersion would be an ideal treatment. On the other hand, for systemic indications such as cardia failure, pulmonary oedema and respiratory distress, the victim may be treated with acetic acid or antivenom. Carukia barnesii: For Irukandji syndrome-associated pain, headache, backache, joint pain, nausea, vomiting, pulmonary oedema, heart failure and, in some cases, intracerebral haemorrhage, treatments include cold packs, seawater compresses, hot water immersion, acetic acid and antibiotic prophylaxis and with severe cases, hospitalization.

7.4.2.3 Preventive Methods of all Jellyfish Stings (Anon. http://www. dermaamin.com/site/atlas-of-dermatology/26-j/ 730-jelly-fish-reaction-.html)

1. Swimming should be done only at patrolled beaches with properly trained lifeguards. 2. Swimming must be avoided in infested waters, especially after a storm, because stings may appear from the remnants of floating damaged tentacles. 3. Apparently dead or beached jellyfish should not be touched. 4. During snorkelling or scuba diving, protective clothing such as a wet suit, long- sleeved shirt, pants or long woollen underwear and glove should be worn. In areas where Irukandji syndrome occurs, a Lycra stinger suit should be worn. 5. Bathing beaches should be closed during periods of high jellyfish infestation or blooms

7.4.2.4 First-Aid Treatment of All Jellyfish Stings

1. The victim should be removed or rescued from the water. 2. Airway, breathing and circulation of the victim should be stabilized. 3. The affected part should be immobilized to prevent further envenomation by adherent tentacles. 4. The type of jellyﬁsh sting should be identiﬁed with the help of subject experts. 5. The nematocysts should be disarmed before removing the adherent tentacles in order to prevent further envenomation of the victim and to reduce the chance of a sting to the rescuer. 310 7 Venomology of Marine Cnidarians

7.4.2.5 Species/Organism-Specific and Follow-Up Treatment of Jellyfish Stings

1. In the case of Chironex ﬂeckeri or other box jellyﬁsh species that cause the Irukandji syndrome are suspected, diluted acetic acid (3–10%) or household vinegar may be doused or sprayed over all areas of tentacle contact for at least 30 s. 2. For sea nettles, water containing sodium bicarbonate (baking soda) may be poured over the affected area or the powder may be applied directly to the tentacles. 3. Methylated spirits or alcohol should not be used in any form to deactivate tentacles as these agents may cause a rapid massive discharge of nematocysts. 4. After the tentacles have been disarmed, they may carefully be removed with a forceps or gently scraped away from the skin with shaving cream and a razor or a plastic card, shell or knife

Secondary infections should be treated with the appropriate parenteral antibiotics, and anti-tetanus therapy should be considered. Application of ice or cold packs can relieve the pain of mild to moderate stings of many types of jellyﬁsh, and aspirin or acetaminophen, alone or in combination with codeine, can be used to relieve persistent pain.

7.4.2.6 Case Study on the Treatment for Jellyfish Sting Taylor (https://www.mja.com.au/system/ﬁles/issues/186_01_010107/tay11043_let ter_fm.pdf) reported on the treatment for jellyﬁsh sting with various agents with victims. Among these agents, hot water and aluminium sulphate showed better results as given below.

Degree of pain relief for the victims after various treatments for jellyﬁsh sting Pain relief during treatment (%) Continuing relief after treatment (%) Treatment Ice 25 2 Vinegar 0 4 Aluminium sulphate 42 21 Hot water 88 88 Source: Taylor https://www.mja.com.au/system/ﬁles/issues/186_01_010107/tay11043_letter_fm. pdf 0 means no relief of pain; 100% means complete relief of pain. The pain relief was temporary (pain returned when treatment stopped) for all except hot water and (to a lesser extent) aluminium sulphate 7.4 Treatment and Management of Marine Cnidarian Envenomations 311

7.4.3 Therapeutic Approaches to Injuries Caused by Sea Anemone Stings

7.4.3.1 First-Aid Measures for Sea Anemone Stings If and when a sea anemone has stung, the victims should be first got out of the water as soon as possible to prevent their drowning. It has been reported that removing any remaining tentacles from the skin is a useful first-aid treatment to prevent further firing of the nematocysts. Washing with vinegar should be avoided after Phyllodiscus semoni stings because vinegar can stimulate nematocysts and further discharges may occur. If nematocysts remain on the skin, the remaining stingers should be gently removed while wearing gloves and the wound washed out with seawater (not freshwater or vinegar) to prevent further stings. It is important to remove the remaining tentacles gently because physical stress such as vibrational stimuli may also stimulate the remaining nematocysts to discharge. After washing, it is better to use hot-water immersion or ice packs on the injured areas as both the treatments are useful. Hot/cold therapy can reduce pain and toxicity through thermolysis; however, they may also result in injury from burns or chilblains. It has also been reported that hot-water immersion method is ideal for pain relief and health improvement after sea anemone envenomation. Envenomation by some other species of sea anemones such as Dofleinia armata, Calliactis polypus and Stichodactyla haddoni has caused cases of dermatitis in mainland Japan. It has also been stated that sea anemone envenomation can sometimes induce dermatitis with swelling and pain. In this case, hot-water immersion (45 C or more for more than 30 min) is recommended for treating injuries. However, if the pain and swelling do not subside, the affected person should visit the hospital (Mizuno 2018).

7.4.3.2 Hospitalization The stings of most cnidarians are either harmless to humans or induce only mild dermatitis, which can usually be treated with either local steroid therapy or oral steroid administration combined with local steroid therapy and/or antihistamine agents. However, when dermatitis is very severe and ulceration and severe swelling occur, oral steroid administration after steroid pulse therapy has been effective in helping patients recover. Prostaglandin E1 agents may also be effective in treating severe dermatitis with necrotizing ulceration by improving local circulation. Because severe swelling in the extremities could result in local circulation failure and compartment syndrome, an incision may be required to relieve the pressure. Depending on the severity of skin ulceration caused by sea anemone stings, skin grafting may also be considered as a treatment choice. As mentioned above, some cases of injury by cnidarians have resulted in flare-ups after initial improvement of inflamed dermatitis. For example in the envenomation of sea anemone Phyllodiscus semoni,aflare-up of dermatitis recurred approximately 2 weeks after initial improvement and the patient remained hospitalized for 21 days. It was reported that pathogenic vibrio infection by bacteria such as Vibrio vulnificus accompanied some cases of injury, resulting in severe sepsis. Although it is possible that injuries from sea anemones can result in secondary infection, administration of the appropriate 312 7 Venomology of Marine Cnidarians antibiotics is effective in treating/preventing secondary infection. Because of the risk of tetanus prophylaxis, the tetanus vaccine (also known as tetanus toxoid) is also suggested as a form of treatment and to prevent tetanus. The Vibrio and other bacteria such as Aeromonas and Pseudomonas can cause secondary infections that can provoke compartment syndrome, but it is not the action of the venom of the anemone (Mizuno 2018).

7.4.3.3 Therapeutic Approaches for Systemic Reactions and Acute Kidney Injury (AKI) There is currently no speciﬁc antivenom or medicine for the envenomation by sea anemones. If any systemic reactions or AKI occur after injury, only conservative therapies are available. In some cases of envenomation by Phyllodiscus semoni with or without systemic reaction, hospitalization of the patients was extended to several months. Most cases kidney injuries involved either direct or indirect acute nebular necrosis caused by cnidarian toxins. The therapeutic approaches for AKI include correcting hypovolemia, haemolysis, rhabdomyolysis, and renal ischaemia through treatments such as systemic shock, as well as correcting vascular ischaemia with adequate infusion therapy. Other supportive therapies, such as the use of diuretics (e.g. furosemides) and vasoregulators (e.g. human atrial natriuretic peptide) and limited use of renal toxic agents, should be considered during the AKI period and recovery phase. In severe cases of AKI with uremic conditions such as azotemia, hyperkalaemia, oliguria (urinary output less than 400–500 mL/day) and anuria (urinary output less than 50–100 mL/day), temporal induction of haemodialysis or peritoneal dialysis should be considered until recovery from uremia.

7.4.3.4 Treatment Measures for Sea Anemone Sting (Anon. https:// www.dovemed.com/diseases-conditions/sea-anemone-sting/) A removal of the tentacles is necessary in the first place, by trapping them in a plaster (sand, talc, shaving foam, etc.) and then scraping them gently. It will then be necessary to cleanse the damaged skin with sea water first, then apply compresses of vinegar (or mixture of acetic acid at 5%), or lime, with the aim of inhibiting the discharge of remaining cnidocysts. Local antihistamines and/or topical corticosteroids may be recommended for severe itching after antisepsis in the area. In the case of coral envenomation which may cause inflammatory dermatitis and chronic infections, the use of antibiotic is recommended (Reese and Depenbrock 2014). The presently adopted treatment measures for sea anemone sting are given below:

1. The ﬁrst line of treatment is often to remove the stingers/spines by gently pulling them out with a pair of tweezers; and breaking the spines must be avoided. 2. Cleaning the affected site with saltwater/seawater and sand may be used to rub the wound and detach stingers. 3. Once the spines (often multiple) are removed, the affected area is washed with soap and water. 4. Application of topical antibiotics (hydrocortisone cream). 7.4 Treatment and Management of Marine Cnidarian Envenomations 313

5. The wound is left uncovered to heal, which may permit the embedded spines to surface. 6. Pain relieving medications as required; vinegar may also be used to reduce pain. 7. Tetanus vaccination is usually required, if it is not up to date. 8. In case of severe stings, it could be a medical emergency and prompt attention has to be provided. The treatment measures may include the following. 9. Cardiopulmonary resuscitation (CPR) may be provided as necessary, breathing assistance. 10. Stabilizing the blood pressure. 11. Pain control medications, steroids. 12. Proper follow-up care and check-ups may be required, especially to monitor for any signs of infection.

Note: It is always important to call the local emergency helpline number without any delay.

7.4.3.5 Preventive Measures of Sea Anemone Sting The following factors may be considered to reduce the incidence of sea anemone stings:

1. Warnings of lifeguards or health ofﬁcials should not be ignored at the beach. 2. It is not advisable to make any attempt to touch or handle marine animals unnecessarily. 3. Protective clothing should be worn if it is planned to swim or dive in infested areas. 4. Protective footwear should be worn while walking on beach sand. 5. Dead sea anemones (since they can also sting) should not be handled if they are found in beaches. 6. When removing stingers from the body, suitable protective cover (such as hand gloves) should be worn; and removing the sting with bare hands should be avoided. 7. Rubbing the stung area with bare (unprotected) hands should be avoided. 8. Safety precautions may be ensured while cleaning marine animal aquariums; use gloves as simple touch of an anemone can trigger its harpoon-like stinging device.

Note: Currently, there is no antivenom available for sea anemone stings.

7.4.3.6 Prognosis of Sea Anemone Sting? (Outcomes/Resolutions)

1. The prognosis of sea anemone sting is generally good with effective treatment since a majority of the cases are mild. However, severe stings combined with delayed treatment may be life-threatening or can even result in death 2. In rare cases, it has been reported that while swimming, detached tentacles of sea anemones may get swallowed, especially while snorkelling 3. Sea anemones are non-aggressive and do not directly attack humans. These creatures are also referred to as “stinging polyps” 314 7 Venomology of Marine Cnidarians

4. The diver will avoid handling or touching the tentacles of the anemones, and will be careful by leaning on the rocks when diving or leaving the water. Wearing thick gloves and slippers makes it possible to touch animals without danger. As tentacles may remain attached to them, the diver will be vigilant during the removal of the mask and snorkel because attacks on the face may appear at that time (very sensitive area of the eyes and mouth).

7.4.4 Treatment of Venomous Hydrozoans

Accidents concerning hydrozoan corals are common in Guadeloupe (France in the Caribbean). The most frequent victims are surfers as well as people practising diving and hunting without protection (combination or lycra). The management of envenomations by ﬁre corals and their prevention are the same as for scyphozoan cnidarians. The management measures include the following:

1. Removal of the remaining cnidocysts using sand plaster or shaving foam, and then delicate scraping using a credit card. 2. Abundant rinsing with seawater (hot if possible because the venom of the ﬁre corals is heat-labile), then disinfection of the area. 3. Symptomatic treatments (antihistamines, analgesics, topical corticosteroids) will be used as well as the veriﬁcation of tetanus vaccination; not to mention the referral to a doctor (antibiotic therapy) for the deepest wounds.

7.4.4.1 Treatment of the Most Important Venomous Hydrozoans Treatment of envenomations by fire coral: Cleansing with seawater may be enough for fire coral-related local (cutaneous) symptoms such as burning/itching, erythema, necrotizing or granulomatous reactions. For systemic symptoms such as mayalgia, fever, malaise, nausea and vomiting, treatment measures such as debride- ment and acetic acid soaks may be followed (Reese and Depenbrock 2014). Management and treatment of envenomations by physalis: As for accidents with other cnidarians, it is necessary first of all to remove the animal to avoid the risk of re-envenomation. If tentacles remain on the skin, they must be removed with a dry sand patch or shaving foam (which will help trap them), then scraped gently with the aid of a rigid surface (piece of cardboard, credit card ...). Then, abundant rinsing will be done with seawater to remove the remaining cnidocysts. Vinegar should not be used because it causes them to burst. The rest of the treatment is identical to that of an envenomation by cnidarians (topical antiseptics and topical cicatrizants, antihistamines and topical corticosteroids, even antalgic by the general way). Cold pack use at the site of the lesions has been shown to be effective against local pain. Serious cases with cardiovascular involvement will require rapid transfer to the hospital with monitoring of pulse rate, respiration rate and blood pressure (Fenner https://www.ilsf.org/sites/ilsf.org/files/filefield/treatmentofmarinestings.pdf). Reese and Depenbrock (2014) reported that the following treatment measure may be ideal for blue bottle envenomations. Cutaneous symptoms (significant oedema and necrosis and pain) of blue bottle stings of Pacific Ocean, Gulf of Mexico and 7.5 Therapeutic Potential of Venom of Marine Cnidarians 315 western Atlantic Ocean may be treated with acetic acid. On the other hand, for systemic symptoms such as abdominal pain, nausea/vomiting, muscular spasm, headache, confusion and respiratory distress (in severe occasions), stingose, backing soda, papain and bromelain, and hot water immersion may be of great use (Reese and Depenbrock 2014).

7.5 Therapeutic Potential of Venom of Marine Cnidarians

Marine cnidarian venoms have been investigated as a potential source of novel bioactive therapeutic compounds (secondary metabolites) which possess various therapeutic activities such as antibacterial, anticancer (cytotoxic), haemolytic and antioxidant.

7.5.1 Role of Cnidarians Venoms in Drug Discovery

Marine invertebrates have been reported to be the rich sources of bioactive compounds and their therapeutic potential attracts scientiﬁc interest worldwide. Although sponges are the foremost providers of marine bioactive compounds, cnidarians are also becoming promising organisms. Among the different groups of cnidarians, anthozoan orders such as Alcyonacea and Gorgonacea display the highest number of species yielding promising pharmaceutical compounds (Santhanam et al. 2019). The chemistry classes of pharmaceutical compounds and their bioactivities studied in marine cnidarians during 2001–2010 are listed below.

Chemistry classes of pharmaceutical compounds in marine cnidarians Terpenoid 61% Steroid 14% Eicosanoid 8% Polyketide 6% Alkaloid 3% Peptide 3% Pyridine 3% Diakylamine 1% Lipid 1% Source: Rocha et al. (2011)

Pharmaceutical activities of bioactive compounds in marine cnidarians Antitumour 41% Antimicrobial 24% Anti-inﬂammatory 22% CNS disorders 2% (continued) 316 7 Venomology of Marine Cnidarians

Antiulcer 1% Others 10% Source: Rocha et al. (2011)

In spite of recent efforts to extract and characterize novel toxins from cnidarians, much more remains to be done to investigate their toxins and their potential as new sources in the development of new drugs. Of the approximately 11,000 cnidarian species, only 156 toxins from 10 pharmacological families have not been defined. Potentially useful new toxicological information is gradually accumulating. One promising solution towards broadening the knowledge on cnidarian toxins is the application of sequencing technologies to identify novel structural and pharmacological groups of toxins. Nevertheless, the enormous potential of cnidarian venoms for understanding the activity of different receptors and channels in health and disease conditions, as well as their use as sources of novel pharmaceutical lead compounds, appears to offer endless possibilities for future scientific research (Jouiaei et al. 2015; Anon. https://www.dermnetnz.org/topics/australian-box-jelly fish-stings/). The toxins of the venoms of the different species of marine cnidarians and their bioactivities are listed below.

7.5.2 Hydrozoan Venoms Possessing Therapeutic Activities

Species Toxin Activity Olindias sambaquiensis Oshem 1,2 Haemolytic Badre (2014) Olindias sambaquiensis Metalloprotease Tissue remodelling Physalia physalis Physalitoxin Haemolytic PpV9.4, PpV19.3 Action on insulin secreting cells Source: Jouiaei et al. (2015) and Mariottini and Pane (2014)

7.5.3 Scyphozoan Venoms Possessing Therapeutic Activities

Species Toxin Activity Cassiopea Crude venom Induces ROS-mediated cytotoxicity andromeda (human breast tumour tissue) Cassiopea Crude venom Against CNS tumours xamachana Chrysaora B phospholipase (PLB2) and Pro/anti-coagulant and pro/anti-thrombotic; fuscescens lysosomal acid lipase; C-type K+ channels blockers lectins (continued) 7.5 Therapeutic Potential of Venom of Marine Cnidarians 317

Chrysaora Crude venom Against human nasopharyngeal carcinoma helvola cell line, CNE-2 Crude venom Against human MCF-7 and CNE-2 tumour cell lines Cotylorhiza Crude venom Cytotoxicity of certain breast cancer cells tuberculata Crude venom In cancer treatments and as antioxidants Cyanea CcTX-1 Cytotoxic capillata Crude venom Haemolytic Cyanea ClGP-1 Cytotoxic lamarkii Crude venom Haemolytic Cyanea Cytotoxicity on H630 cells nozakii Nemopilema Crude venom Cytotoxicity of HepG2 cells; promising nomurai target for hepatocellular carcinoma therapeutics Mucin For treating joint disease such as osteoarthritis Crude venom Haemolytic Pelagia Crude venom Haemolytic noctiluca Rhizostoma Crude venom Haemolytic pulmo Rhopilema Protein Antioxidant Wikipedia esculentum Rhopilema PLA2 Biosynthesis of prostaglandin nomadica Stomolophus SmP90 Radical scavenging (antioxidant) meleagris Source: Jouiaei et al. (2015), Mariottini and Pane (2014), and Anon. https://www.theguardian.com/ environment/2013/jun/03/jellyﬁsh-surge-mediterranean-environment-tourists

7.5.4 Cubozoan Venoms Possessing Therapeutic Activities

Species Toxin Activity Carybdea alata CaTX-A,B Haemolytic/lethal Carybdea marsupialis CARTOX, cytolysins Haemolytic/lethal Carybdea rastonii CrTX-A, CrTX-I, CrTX-II and CrTX-III Haemolytic/lethal Chironex ﬂeckeri CTX-1,2,A,B Cytotoxic, haemolytic Venom proteins Haemolytic Chiropsalmus quadrigatus CqTX-A, haemolysin Cytolytic, haemolytic Source: Jouiaei et al. (2015) and Mariottini and Pane (2014) 318 7 Venomology of Marine Cnidarians

7.5.5 Anthozoan Venoms Possessing Therapeutic Activities

7.5.5.1 Sea Anemone (Actiniaria) Toxins Possessing Therapeutic Activities Species Toxin Activity Actinia equina Equinatoxin Antitumoural Actinia equina EqTx-II Against human U87 glioblastoma; A172 014 Actinia equina EqTx-II Against V-79-379, a normal lung fibroblasts of Chinese hamster Actinia equina EqTx-II -I18C mutant Against human MCF 7 breast adenocarcinoma; ZR 751 breast carcinoma; HT 1080 fibrosarcoma Actinia equina Crude venom Against V79 normal lung fibroblasts of Chinese hamster Aiptasia Crude venom Haemolytic mutabilis Aiptasia Crude venom Against monkey Vero normal kidney cells; and mutabilis human Hep-2 epithelial carcinoma Anemonia Crude venom Against V79 normal lung fibroblasts of Chinese sulcata hamster Anthopleura Pore-forming protein Haemolytic, anticancer; cytotoxic in A549 cells dowii Anthopleura Peptide and protein Cytolytic fuscoviridis toxins (cytolysins) Anthopleura Peptide and protein Cytolytic japonica toxins (cytolysins) Anthopleura Peptide and protein Cytolytic michaelseni toxins (cytolysins) Anthopleura Peptide and protein Cytolytic xanthogrammica toxins (cytolysins) Bunodosoma Bc2 Against human U87 glioblastoma; A172 caissarum glioblastoma Bunodosoma Peptide and protein Cytolytic caissarum toxins (cytolysins) Bunodosoma Bunodosine 391 Analgesic cangicum Bunodosoma Peptide and protein Cytolytic capensis toxins (cytolysins) Condylactis Peptide and protein aurantiaca toxins (cytolysins) cytolytic Entacmaea Peptide and protein Cytolytic quadricolor toxins (cytolysins) Epiactis Peptide and protein Cytolytic japonica toxins (cytolysins) Epiactis Peptide and protein Cytolytic prolifera toxins (cytolysins) Heteractis Peptide and protein Cytolytic aurora toxins (cytolysins) (continued) 7.5 Therapeutic Potential of Venom of Marine Cnidarians 319

Heteractis Peptide and protein Cytolytic crispa toxins (cytolysins) Heteractis Actinoporin RTX-A Against human HL-60 promyelocytic leukaemia; crispa HeLa Cervix carcinoma; THP-1 monocytic leukaemia; MDA-MB-231 breast cancer; SNU-C4 colon cancer Heteractis Actinoporins Serve as cell lysis buffers crispa Heteractis Crude venom Against human lung and breast cancer cells, magniﬁca A549 cells Heteractis Peptide and protein Cytolytic magniﬁca toxins (cytolysins) Metridium senile Metridiolysin Haemolytic Metridium senile Peptide and protein Cytolytic toxins (cytolysins) Palythoa Palytoxin Against human UKHN-1 (oropharynx squamous caribaeorum cell carcinoma), UKHN-2 (Oesophagus squamous cell carcinoma), UKHN-3 (tongue squamous cell carcinoma) Palythoa Palytoxin For treatment of heart disease, high blood caribaeorum pressure and other diseases Palythoa Palytoxin Anticancer heliodiscus Palythoa liscia Palystatins A-D Against mouse P388 Lymphoma Palythoa Palytoxin Against human H2981 lung adenocarcinoma tuberculosa Paracondylactis Peptide and protein Cytolytic sinensis toxins (cytolysins) Phymactis Peptide and protein Cytolytic clematis toxins (cytolysins) Pseudactinia Peptide and protein Cytolytic infecunda toxins (cytolysins) Pseudactinia Peptide and protein Cytolytic varia toxins (cytolysins) Sagartia elegans Src I Haemolytic Acidic actinoporin Src I Against human U251 glioblastoma; NSCLC non-small cell lung carcinoma; BEL-7402 liver carcinoma; BGC-823 stomach adenocarcinoma Stichodactyla Crude venom Haemolytic haddoni Stichodactyla Peptide and protein cytolytic gigantea toxins (cytolysins) Stichodactyla Sticholysins I and II Neuroactive and cardioactive properties helianthus (St I/II) (cytolysins) Stichodactyla ShK and ShK-186 Potassium channel blocker; for treatment of helianthus (dalazatide) autoimmune diseases Bc2, EqTX-II, PTX-A Anticancer property and sticholysin I (continued) 320 7 Venomology of Marine Cnidarians

Crude venom Haemolytic Stichodactyla Peptide and protein Cytolytic helianthus toxins (cytolysins) Stichodactyla Peptide and protein Cytolytic mertensii toxins (cytolysins) Urticina eques Ueq 12-1 Antibacterial against the Gram-positive strain Corynebacterium glutamicum; analgesic and anti-inﬂammatory effects; antinociceptive Urticina eques Peptide and protein Cytolytic toxins (cytolysins) Urticina felina Peptide and protein Cytolytic toxins (cytolysins) Urticina UpI (protein) Against human KB epidermoid carcinoma; piscivora HEL299 embryonic lung; haemolytic Urticina Peptide and protein Cytolytic piscivora toxins (cytolysins) Source: Jouiaei et al. (2015) and Mariottini and Pane (2014)

7.5.5.2 Soft Coral (Alcyonacea) Toxins Possessing Therapeutic Activities Species Toxin Activity Sarcophyton trocheliophorum Crude venom Cytotoxic, haemolytic Source: Jouiaei et al. (2015), Mariottini and Pane (2014), and Santhanam et al. (2019) References

Ager OED (2008) Actinia equina Beadlet anemone. Tyler-Walters H, Hiscock K (eds) Marine life information network: biology and sensitivity key information reviews. https://www.marlin.ac. uk/species/detail/1561. Accessed 11 Jul 2019 Al-Rubiay KK, Al-Musaoi HA, Alrubaiy L, Al-Freje MG (2009) Skin and systemic manifestations of Jellyfish stings in Iraqi fishermen. Libyan J Med 4:75–77 Anderluh G, Macek P (2012) Cytolytic peptide and protein toxins from sea anemones (Anthozoa: Actiniaria). Toxicon 40:111–124 Anderson N (2014) Two new extremely venomous Irukandji jellyfish discovered in Australia. Sci News. http://www.sci-news.com/biology/science-keesingia-gigas-malo-bella-two-new- extremely-venomous-irukandji-jellyfish-australia-02099.html Accessed 11 Jul 2019 Arai NA (1997) A functional biology of scyphozoa. Chapman & Hall, New York. 316 p Assaw S, Ahmad AS, Wahid MEA (2016) Potential of Malaysian white type edible jellyfish, Lobonema smithii as antioxidant and collagen promoter in dermal wound of Sprague Dawley rats. Middle East J Sci Res 24:2137–2144 Babenko VV, Mikov AN, Manuvera VA, Anikanov NA, Kovalchuk SI, Andreev YA, Logashina YA, Daniil A, Kornilov DA, Manolov AI, Sanamyan NP, Sanamyan KE, Kostryukova ES, Kozlov SA, Grishin EV, Govorun VM, Lazarev VN (2017) Identification of unusual peptides with new Cys frameworks in the venom of the cold-water sea anemone Cnidopus japonicus. Sci Rep 7:14534 Bambaradeniya CNB, Karunaratne DMSS (eds) (2006) The fauna of Sri Lanka: status of taxonomy, research, and conservation. IUCN Sri Lanka and the Government of Sri Lanka, Colombo. 308 p Barceloux DG (2008) Medical toxicology of natural substances: foods, fungi, medicinal herbs, plants, and venomous animals. WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim. 1157 p Bellomio A, Morante K, Barlic A, Gutiérrez-Aguirre I, Viguera AR, González-Mañas JM (2009) Purification, cloning and characterization of fragaceatoxin C, a novel actinoporin from the sea anemone Actinia fragacea. Toxicon 54:869–880 Ben-Ari H, Paz M, Sher D (2018) The chemical armament of reef-building corals: inter- and intraspecific variation and the identification of an unusual actinoporin in Stylophora pistilata. Sci Rep 8:251 Bengtson K, Nichols MM, Schnadig V, Ellis MD (1991) Sudden death in a child following jellyfish envenomation by Chiropsalmus quadrumanus. Case report and autopsy findings. J Am Med Assoc 266:1404–1406 Bentlage B (2013) Description of the chirodropid box jellyfish Chiropsella rudloei sp. nov. (Cnidaria: Cubozoa) from Madagascar. Mar Biodivers Rec 6:e118 Bentlage B, Cartwright P, Yanagihara AA, Lewis C, Richards GS, Collins AS (2010) Evolution of box jellyfish (Cnidaria: Cubozoa), a group of highly toxic invertebrates. Proc Biol Sci 277:493–501 Bernheimer AW, Avigad LS, Branch G, Dowdle E, Lai CY (1984) Purification and properties of a toxin from the South African sea anemone, Pseudactinia varia. Toxicon 22:183–191

# Springer Nature Singapore Pte Ltd. 2020 321 R. Santhanam, Biology and Ecology of Venomous Marine Cnidarians, https://doi.org/10.1007/978-981-15-1603-0 322 References

Blaxter JHS, Russell SFS, Yonge SM (eds) (1984) Advances in marine biology, vol 21. Academic Press, London. 238 p Bordehore C, Nogué S, Gili JM, Acevedo MJ, Fuentes VL (2015) Carybdea marsupialis (Cubozoa) in the Mediterranean Sea: the first case of a sting causing cutaneous and systemic manifestations. J Travel Med 22:61–63 Bowles D, Swaby J, Harlan H (2018) Guide to venomous and medically important invertebrates. CSIRO Publishing, Clayton South, VIC. 240 p Brinkman DL, Konstantakopoulos N, McInerney BV, Mulvenna J, Seymour JE, Isbister GK, Hodgson WC (2014) Chironex fleckeri (box jellyfish) venom proteins: expansion of a cnidarian toxin family that elicits variable cytolytic and cardiovascular effects. J Biol Chem 289:4798–4812 Brough C, McBirney C (2015) Saddle anemone—carpet anemone. Animal-world. http://animal- world.com/Aquarium-Coral-Reefs/Saddle-Anemone. Accessed 11 Jul 2019 Bruhn T, Schaller C, Schulze C, Sanchez-Rodriguez J, Dannmeier C, Ravens U, Heubach JF, Eckhardt K, Schmidtmayer J, Schmidt H, Aneiros A, Wachter E, Béress L (2001) Isolation and characterisation of five neurotoxic and cardiotoxic polypeptides from the sea anemone Anthopleura elegantissima. Toxicon 39:693–702 Burnett JW, Fenner PJ, Rifkin JF (1996) Venomous and poisonous marine animals: a medical and biological handbook. University of New South Wales Press, Sydney. 504 p Cadogan M (2019) Box jellyfish (Chironex fleckeri). https://litfl.com/box-jellyfish-chironex- fleckeri/ Calton GJ, Burnett JW, Vader W (1978) A study of the nematocyst venoms of the sea anemone, Bolocera tuediae. Toxicon 16:443–451 Carett TJ, Underwood AH, Seumour JE (2012) 2012.Irukandji syndrome: a widely misunderstood and poorly researched tropical marine envenoming. Diving Hyperb Med 42:214–223 Cariello L, Santis AD, Fiore F, Piccoli R, Spagnuolo A, Zanetti L, Parente A (1989) Calitoxin, a neurotoxic peptide from the sea anemone Calliactis parasitica: amino-acid sequence and electrophysiological properties. Biochemistry 28:2484–2489 Cegolon L, Heymann WC, Lange JC, Mastrangelo G (2013) Jellyfish stings and their management: a review. Mar Drugs 11:523–550 Chaiyakul T (2017) Jellyfish envenomation in Thailand: field and prehospital management. Royal Thai Navy Med J 44:199–206 Cline EI, Wiebe LI, Young JD, Samuel J (1995) Toxic effects of the novel protein UPI from the sea anemone Urticina piscivora. Pharmacol Res 32:309–314 Collins AG, Bentlage B, Gillan W, Lynn TH, Morandini AC, Marques AC (2011) Naming the Bonaire banded box jelly, Tamoya ohboya, n. sp. (Cnidaria: Cubozoa: Carybdeida: Tamoyidae). Zootaxa 2753:53–68 Columbus-Shenkar YY, Sachkova MY, Macrander J, Fridrich A, Modepalli V, Reitzel AM, Sunagar K, Moran Y (2018) Dynamics of venom composition across a complex life cycle. elife 7:e35014 Cooke TS, Halstead BW (1970) Report of stingings by the coelenterate Rhizophysa eysenhardti gegenbaur in California waters. J Clin Toxicol 3:589–595 Culver P, Jacobs RS (1981) Lophotoxin, a neuromuscular acting toxin from the sea whip Lophogorgia rigida. Toxicon 19:825–830 Deeds JR, Handy SM, White KD, Reimer JD (2011) Palytoxin found in Palythoa sp. zoanthids (Anthozoa, Hexacorallia) sold in the home aquarium trade. PLoS One 6:e18235 Diochot S, Loret E, Bruhn T, Béress L, Lazdunski M (2003) APETx1, a new toxin from the sea anemone Anthopleura elegantissima, blocks voltage-gated human ether-a-go-go-related gene potassium channels. Mol Pharmacol 64:59–69 Dodson SI, Cooper SD (1983) Trophic relationships of the freshwater jellyfish Cruspedacusta sowerbyi Lankester 1880. Limnol Oceanogr 28(1983):345–351 Dong Z, Liu D, Keesing JK (2010) Jellyfish blooms in China: dominant species, causes and consequences. Mar Pollut Bull 60:954–963 References 323

Due K (2017) Australian box jellyfish stings. https://www.dermnetnz.org/topics/australian-box- jellyfish-stings/. Accessed 11 Jul 2019 Fenical W, Okuda RK, Bandurraga MM, Culver P, Jacobs RS (1981) Lophotoxin: a novel neuromuscular toxin from Pacific sea whips of the genus Lophogorgia. Science 212:1512–1514 Fenner P (1997) Awareness, Prevention and Treatment of world-wide marine stings and bites. https://www.ilsf.org/sites/ilsf.org/files/filefield/treatmentofmarinestings.pdf. Accessed 11 Jul 2019 Fenner PJ (2005) Venomous jellyfish of the world. SPUMSJ 35:131–138 Frazão B, Vasconcelos V, Antune A (2012) Sea anemone (Cnidaria, Anthozoa, Actiniaria) toxins: an overview. Mar Drugs 10:1812–1851 Frazão B, Antunes A (2016) Jellyfish bioactive compounds: methods for wet-lab work. Mar Drugs 14:75 Fujita S, Warashina A, Satake M (1983) Binding characteristics of a sea anemone toxin from Parasicyonis actinostoloides with crayfish leg nerves. Comp Biochem Physiol C Toxicol Pharmacol 76:25–32 Gacesa R, Chung R, Dunn SR, Weston AJ, Jaimes-Becerra A, Marques AC, Morandini AC, Hranueli D, Starcevic A, Ward M, Long PF (2015) Gene duplications are extensive and contribute significantly to the toxic proteome (a proteome is the complete set of proteins expressed by an organism) of nematocysts isolated from Acropora digitifera (Cnidaria: Anthozoa: Scleractinia). BMC Genomics 16:774 García-Arredondo A, Murillo-Esquivel LJ, Rojas A, Sanchez-Rodriguez J (2014) Characteristics of hemolytic activity induced by the aqueous extract of the Mexican fire coral Millepora complanata. Incl Trop Dis 20:49 Gershwin L (2007) Malo kingi: a new species of Irukandji jellyfish (Cnidaria: Cubozoa: Carybdeida), possibly lethal to humans, from Queensland, Australia. Zootaxa 1659:55–68 Gershwin L (2008) Morbakka fenneri, a new genus and species of Irukandji jellyfish (Cnidaria: Cubozoa), Memoirs of the Queensland Museum. Nature 54(1):23–33 Gershwin L, Gibbons MJ (2009) Carybdea branchi, sp. nov., a new box jellyfish (Cnidaria: Cubozoa) from South Africa. Zootaxa 2088:41–50 Gershwin L, Alderslade P (2006) Chiropsella bart n. sp., a new box jellyfish (Cnidaria: Cubozoa: Chirodropida) from the Northern Territory, Australia. The Beagle 22:15–21 Gibbons W, Haynes RR, Thomas JL (1990) Poisonous plants and venomous animals of Alabama and adjoining states. The University of Alabama Press, Alabama. 368 p Goemans B (2012a) Palythoa tuberculosa. Saltcorner. http://www.saltcorner.com/ AquariumLibrary/browsespecies.php?CritterID¼2148. Accessed 11 Jul 2019 Goemans B (2012b) Saltcorner. http://www.saltcorner.com/AquariumLibrary/browsespecies.php? CritterID¼2299. Accessed 11 Jul 2019 Haddad V Jr, Silveira FL, Cardoso JLC, Morandin AC (2002) A report of 49 cases of cnidarian envenoming from southeastern Brazilian coastal waters. Toxicon 40:1445–1450 Haddad V Jr, Zara F, Marangoni S, Toyama DO, de Souza AJF, de Oliveira SCB, Toyama MH (2014) Identification of two novel cytolysins from the hydrozoan Olindias sambaquiensis (Cnidaria). J Venom Anim Toxins Incl Trop Dis. 20:10 Hale G (1999) The classification and distribution of the class scyphozoa. https://gladstone.uoregon. edu/~ghale/pdf/scyphozoa.pdf. Accessed 11 Jul 2019 Häussermann V, Försterra G (2001) A new species of sea anemone from Chile, Anemonia alicemartinae n. sp. (Cnidaria: Anthozoa). An invader or an indicator for environmental change in shallow water? Org Divers Evol 1:211–224 Hernández-Matehuala R, Rojas-Molina A, Vuelvas-Solórzano AA, Garcia-Arredondo A, Alvarado CI, Olguín-López N, M (MA (2015) Cytolytic and systemic toxic effects induced by the aqueous extract of the fire coral Millepora alcicornis collected in the Mexican Caribbean and detection of two types of cytolisins. J Venom Anim Toxins Incl Trop Dis 21:36 Hoffmann K, Hermanns-Clausen M, Buhl C, Kauferstein S (2008) A case of palytoxin poisoning due to contact with zoanthid corals through a skin injury. Toxicon 51(8):1535–1537 324 References

Honma T, Hasegawa Y, Ishida M, Nagai H, Nagashima Y, Shiomi K (2005) Isolation and molecular cloning of novel peptide toxins from the sea anemone Antheopsis maculata. Toxicon 45:33–41 Horiike T, Nagai H, Kitani S (2015) Identification of allergens in the box jellyfish Chironex yamaguchii that cause sting dermatitis. Int Arch Allergy Immunol 167:73–82 Houck HE, Lipsky MM, s Marzella L, Burnett JV (1996) Toxicity of sea nettle (Chrysaora quinquecirrha) fishing tentacle nematocyst venom in cultured rat hepatocytes. Toxicon 34 (7):771–778 Hu B, Guo W, Wang L, Jiao B, Wang J, Liu X (2011) Purification and characterization of gigantoxin-4, a new actinoporin from the sea anemone Stichodactyla gigantea. Int J Biol Sci 7(6):729–739 Ibarra-Alvarado C, García JA, Aguilar MB, Rojas A, Falcón A, de la Cotera EPH (2007) Biochem- ical and pharmacological characterization of toxins obtained from the fire coral Millepora complanata. Comp Biochem Physiol Part C 146(2007):511–518 Il’ina AP, Monastyrsnaia MM, Sokotun IN, Egorov TA, Nazarenko YA, Likhatskaia GN, Kozlovskaia EP (2005) Actinoporins from the sea of Japan anemone Oulactis orientalis: isolation and partial characterization. Bioorg Khim 31:39–48 Imani M, Jaliani HZ, Kheirandish MH, Azadpour M (2017) Recombinant production and affinity purification of the FraC pore forming toxin using hexa-His tag and pET expression cassette. Iran J Basic Med Sci 20:380–385 Inman WJ (2018) Jellyfish numbers on the rise along US beaches. https://wwwfoxnewscom/ science/jellyfish-numbers-on-the-rise-along-us-beaches. Accessed 11 Jul 2019 Jouiaei M (2016) Evolution and diversification of the cnidarian venom system. Doctor of Pharmacy (Pharm.D) Thesis, The University of Queensland, Australia Jouiaei M, Yanagihara AA, Madio B, Nevalainen TJ, Alewood PF, Fry BG (2015a) Ancient venom systems: a review on cnidaria toxins. Toxins 7:2251–2271 Jouiaei M, Sunagar K, Gross AF, Scheib H, Alewood PF, Moran Y, Fry BG (2015b) Evolution of an ancient venom: recognition of a novel family of cnidarian toxins and the common evolution- ary origin of sodium and potassium neurotoxins in sea anemone. Mol Biol Evol 32:1598–1610 Kawabata T, Lindsay DJ, Kitamura M, Konishi S, Nishikawa J, Nishida S, Kamio M, Nagai H (2013) Evaluation of the bioactivities of water-soluble extracts from twelve deep-sea jellyfish species. Fish Sci 79:487–494 Kawahara M, Dawson MN (2007) Jellyfish feature. http://thescyphozoan.ucmerced.edu/Org/JotQ/ JotQ_07Aug.html. Accessed 11 Jul 2019 Kawahara M, Uye S, Burnett J, Mianzan H (2006) Stings of edible jellyfish (Rhopilema hispidum, Rhopilema esculentum and Nemopilema nomurai) in Japanese waters. Toxicon 48:713–7136 Kelso GJ, Blumenthal KM (1998) Identification and characterization of novel sodium channel toxins from the sea anemone Anthopleura xanthogrammica. Toxicon 36:41–51 Kennedy J (2019) Learn about the blue button jelly. https://wwwthoughtcocom/blue-button-jelly- porpita-porpita-2291819. Accessed 11 Jul 2019 Kitatani R, Yamada M, Nagai MK (2015) Length is associated with pain: jellyfish with painful sting have longer nematocyst tubules than harmless jellyfish. PLoS One 10:e0135015 Kye (2014) 7 Most deadliest, Most poisonous jellyfish in the world conservation institute. https:// wwwconservationinstituteorg/7-deadliest-poisonous-jellyfish-world/. Accessed 11 Jul 2019 Lagos P, Duran R, Cerveñansky C, Freitas JC, Silveira R (2001) Identification of hemolytic and neuroactive fractions in the venom of the sea anemone Bunodosoma cangicum. Braz J Med Biol Res 34:895–902 Lakkis NA, Maalouf GJ, Mahmassani DM (2015) Jellyfish stings: a practical approach. Wilderness Environ Med 26:422–429 Lawley JW, Faria E Jr (2018) First record of association between Tamoya haplonema (Cnidaria: Cubozoa) and stromateid fish, with a review on interactions between fish and cubozoan jellyfishes. Plankton Benthos Res 13:32–38 References 325

Lazcano-Pérez F, Castro H, Arenas I, García DE, González-Muñoz R, Arreguín-Espinosa R (2016) Activity of Palythoa caribaeorum venom on voltage-gated ion channels in mammalian superior cervical ganglion neurons. Toxins 8:135 Leverenz E (2000) Pelagia noctiluca. Animal diversity web. https://animaldiversity.org/accounts/ Pelagia_noctiluca/. Accessed 11 Jul 2019 Levy S, Masry D, Halstead BW (1971) Report of stingings by the sea anemone Triactis producta Klunzinger from Red Sea. Clin Toxicol 3:637–643 Li R, Yu H, Yue Y, Liu S, Xing R, Chen X, Li P (2016) Combined proteomics and transcriptomics identifies sting-related toxins of jellyfish Cyanea nozakii. J Proteome 148:57–64 Logashina YA, Solstad RG, Mineev KS, Korolkova YV, Mosharova IV, Dyachenko IA, Palikov VA, Palikova YA, Murashev AN, Arseniev AS, Kozlov SA, Stensvåg K, Haugd T, Andree YA (2017) New disulfide-stabilized fold provides sea anemone peptide to exhibit both antimicrobial and TRPA1 potentiating properties. Toxins 9:154 Loh YY (2011) Actinia tenebrosa. (Farquhar1898) Invertebrates of the Coral Sea. https://www. gbri.org.au/Species/Actiniatenebrosa.aspx?PageContentID¼1484. Accessed 11 Jul 2019 Maček P (1992) Polypeptide cytolytic toxins from sea anemones (Actiniaria). FEMS Microbiol Immunol 5:121–129 Macrander J, Daly M (2016) Evolution of the cytolytic pore-forming proteins (Actinoporins) in sea anemones. Toxins (Basel) 8, pii: E368 Madio B, . King GF, Undheim EAB (2019) Sea anemone toxins: a structural overview Mar Drugs 17: 325 Maldonado E, Maillaud C, Barguil Y, Labadie M (2017) Rhabdomyolysis during envenomation by Physalia sp envenomation in New Caldonia. Med Sante Trop 27:105–108 Malpezzi ELA, Freitas JC, Muramoto K, Kamiya H (1993) Characterization of peptides in sea anemone venom isolated by a novel procedure. Toxicon 31:853–864 Manning E (1997) Glow fish. Bioscience 47:135–138 Maretić Z, Russell FE (1983) Stings by sea Anemonia sulcata in the Adriztc Sea. Am J Trop Med Hyg 32:891–896 Mariottini GL, Pane L (2010) Mediterranean jellyfish venoms: a review on scyphomedusae. Mar Drugs 8:1122–1152 Mariottini GL (2014) Hemolytic venoms from marine cnidarian jellyfish—an overview. J Venom Res 5:22–32 Mariottini GL, Pane L (2014) Cytotoxic and cytolytic cnidarian venoms. A review on health implications and possible therapeutic applications. Toxins 6:108–151 Mariottini GL, Grice ID (2016) Antimicrobials from cnidarians. A new perspective for anti- infective therapy? Mar Drugs 14:48 Mariscal RN, McLean RB, Hand C (1977) The form and function of cnidarian spirocysts. 3. Ultrastructure of the thread and the function of spirocysts. Cell Tissue Res 178:427–433 Marques AC, Haddad V Jr, Migotto AE (2002) Envenomation by a benthic hydrozoa (Cnidaria): the case of Nemalecium lighti (Haleciidae). Toxicon 40:213–215 Marques AC, Haddad V Jr, Rodrigo L, Marques-da-Silva E, Morandini AC (2014) Jellyfish (Chrysaora lactea, Cnidaria, Semaeostomeae) aggregations in southern Brazil and consequences of stings in humans. Lat Am J Aquat Res 42:1194–1199 Marsh LM, Slack-Smith S (2010) Field guide to sea stingers and other venomous and poisonous marine invertebrates of Western Australia. Western Australian Museum Welshpool., 244 p Martin EJ (1960) Observations on the toxic sea anemone, Rhodactis howesii (Coelenterata). Pac Sci 14:403–407 Mayer AG (1910) Medusae of the world, III: the Scyphomedusae. Carnegie Institute, Washington, DC Meinardi E, Azcurra JM, Florin-Christensen M, Florin-Christensen J (1994) Coelenterolysin: a hemolytic polypeptide associated with the coelenteric fluid of sea anemones. Comp Biochem Physiol B Biochem Mol Biol 109:153–161 Mercurio S (2016) Understanding toxicology. Jones & Bartlett Publishers, Burlington, MA. 952 p 326 References

Mianzan H, Sorarrain D, Á Burnett JW, Lutz LL (2000) Mucocutaneous junctional and flexural paresthesias caused by the holoplanktonic trachymedusa Liriope tetraphylla. Dermatology 201:46–48 Mizuno M (2018) Nephrotoxic effects of venoms from sea anemones from Japan. In: Stiles B, Alape-Girón BA, Dubreuil JD, Mandal M (eds) Microbial toxins. Springer Science+Business Media, Berlin, pp 1–13 Mizuno M, Ito Y, Morga BP (2012) Exploiting the nephrotoxic effects of venom from the sea anemone, Phyllodiscus semoni, to create a hemolytic uremic syndrome model in the rat. Mar Drugs 10:1582–1604 Mizuno M, Nozaki M, a Morine N, Suzuki N, Nishikawa K, Morgan BP, Matsuo S (2007) A protein toxin from the sea anemone Phyllodiscus semoni targets the kidney and causes a severe renal injury with predominant glomerular endothelial damage. Am J Pathol 171:402–414 Mizuno M, Nishikawa K, Yuzawa Y, Kanie T, Mori H, Araki Y, Hotta N, Matsuo S (2000) Acute renal failure after a sea anemone sting. Am J Kidney Dis 36:E10 Montgomery L, Seys J, Mees J (2016) To pee, or not to pee: a review on envenomation and treatment in European jellyfish species. Mar Drugs 14:127 Morabito R, Costa R, Rizzo V, Remigante A, Nofziger C, La Spada G, Marino A, Paulmichl M, Dossen S (2017) Crude venom from nematocysts of Pelagia noctiluca (Cnidaria: Scyphozoa) elicits a sodium conductance in the plasma membrane of mammalian cells. Sci Rep 7:41065 Mustafa MR, White E, Hongo K, Othman I, Orchard CH (1995) The mechanism underlying the cardiotoxic effect of the toxin from the jellyfish Chironex fleckeri. Toxicol Appl Pharmacol 133:196–206 Nagai H, Oshiro N, Takuwa-Kuroda K, Iwanaga S, Nozaki M, Nakajima T (2002) A new polypeptide toxin from the nematocyst venom of an Okinawan sea anemone Phyllodiscus semoni (Japanese name “unbachi-isoginchaku”). Biosci Biotechnol Biochem 66:2621–2625 Nagata RM, Haddad MA, Nogueira M Jr (2009) The nuisance of medusae (Cnidaria, Medusozoa) to shrimp trawls in central part of southern Brazilian Bight, from the perspective of artisanal fishermen. Pan-Am J Aquat Sci 4:312–325 Nedosyko AM, Young JE, Edwards JW, da Silva KB (2014) Searching for a toxic key to unlock the mystery of anemonefish and anemone symbiosis. PLoS One 9:e98449 Ne’eman I, Fishelson L, Kashman Y (1975) Sarcophine—a new toxin from the soft coral Sarcophyton glaucum (Alcyonaria). Toxicon 12:593–598 Nellis DW (1997) Poisonous plants and animals of Florida and the Caribbean. Pineapple Press, Inc, Sarasota, FL. 416 p Nevalainen TJ, Peuravuori HJ, Quinn RJ, Llewellyn LE, Benzie JA, Fenner PJ, Winkel KD (2004) Phospholipase A2 in cnidaria. Comp Biochem Physiol B Biochem Mol Biol 139:731–735 Nordesjö A (2016) Treatment of Lion’s Mane jellyfish stingshot water immersion versus topical corticosteroids. https://gupea.ub.gu.se/bitstream/2077/54217/1/gupea_2077_54217_1.pdf Oiso N, Fukai K, Ishii M, Ohgushi T, Kubota S (2005) Jellyfish dermatitis caused by Porpita pacifica, a sign of global warming? Contact Dermat 52:232–233 Oliveira JS, Zaharenko AJ, Ferreira WA Jr, Konno K, Shida CS, Richardson M, Lúcio AD, Beirão PS, de Freitas JC (2006) BcIV, a new paralyzing peptide obtained from the venom of the sea anemone Bunodosoma caissarum. A comparison with the Na+ channel toxin BcIII. Biochim Biophys Acta 1764:1592–1600 Orts DJB, Peigneur S, Silva-Gonçalves LC, Arcisio-Miranda M, Bicudo JEPW, Tytgat J (2018) AbeTx1 is a novel sea anemone toxin with a dual mechanism of action on shaker-type K+ channels activation. Mar Drugs 16:360 Orts DJB, Moran Y, Cologna CT, Peigneur S, Madio B, Praher D, Quinton L, Pauw ED, Bicudo JEPW, Tytgat J, de Freitas JC (2013) BcsTx3 is a founder of a novel sea anemone toxin family of potassium channel blocker. FEBS J 280:4839–4852 Oshiro N, Kobayashi C, Iwanaga S, Nozaki M, Namikoshi M (2004) A new membrane-attack complex/perforin (MACPF) domain lethal toxin from the nematocyst venom of the Okinawan sea anemone Actineria villosa. Toxicon 43:225–228 References 327

Oskin B (2015) Billions of blue jellyfish setting sail for beaches. Live Science. https://www. livescience.com/50965-velella-blue-jellyfish-summer-2015.html. Accessed 11 Jul 2019 O’Sullivan K (2017) Stinger jellyfish swarms wipe out farmed salmon in west of Ireland. https:// www.irishtimes.com/news/environment/stinger-jellyfish-swarms-wipe-out-farmed-salmon-in- west-of-ireland-1.3247245 Paramasivam N, Ben-Dov E, Arotsker L, Kramarsky-Winter E, Zvuloni A, Loya Y, Kushmaro A (2013) Bacterial consortium of Millepora dichotoma exhibiting unusual multifocal lesion event in the Gulf of Eilat, Red Sea. Microb Ecol 65:50–59 Patocka J, Gupta RC, Wu Q, Kuca K (2015) Toxic potential of palytoxin. J Huazhong Univ Sci Technol Med Sci 35:773–780 Pereira JCC, Szpilman D, Haddad V Jr (2018) Anaphylactic reaction/angioedema associated with jellyfish sting. Rev Soc Bras Med Trop 51:1–3 Pigulevsky SV, Michaleff PV (1969) Poisoning by the medusa Gonionemus vertens in the Sea of Japan. Toxicon 7:145–149 Ponce D, Brinkman DL, Potriquet J, Mulvenna J (2016) Tentacle transcriptome and venom proteome of the Pacific sea nettle, Chrysaora fuscescens (Cnidaria: Scyphozoa). Toxins 8:102 Ponce D, Brinkman DL, Ramirez L, Karen LR, Wright CE, Dorantes-Aranda JJ (2015) Compara- tive study of the toxic effects of Chrysaora quinquecirrha (Cnidaria: Scyphozoa) and Chironex fleckeri (Cnidaria: Cubozoa) venoms using cell-based assays. Toxicon 106:57–67 Ponce D, López-Vera E, Aguilar MB, J Sánchez-Rodríguez J (2013) Preliminary results of the in vivo and in vitro characterization of a tentacle venom fraction from the jellyfish Aurelia aurita. Toxins 5:2420–2433 Prentis PJ, Pavasovic A, Norton RS (2018) Sea anemones: quiet achievers in the field of peptide toxins. Toxins 10:36 Qu X, Fan L, Zhong T, Li G, Xia X, Long H, Huang D, Shu W (2016) The nematocysts venom of Chrysaora helvola Brandt leads to apoptosis-like cell death accompanied by uncoupling of oxidative phosphorylation. Toxicon 110:74–78 Radwan F (2002) Comparative toxinological and immunological studies on the nematocyst venoms of the Red Sea fire corals Millepora dichotoma and M.platyphylla. Comp Biochem Physiol C Toxicol Pharmacol 131:323–334 Radwan FF, Aboul-Dahab HM, Burnett JW (2002) Some toxicological characteristics of three venomous soft corals from the Red Sea. Comp Biochem Physiol C Toxicol Pharmacol 132:25–35 Radwan FF, Gershwin L, Burnett JW (2000) Toxinological studies on the nematocyst venom of Chrysaora achlyos. Toxicon 38:1581–1591 Raghubir R, Mishra V, Samuel SS, Lakshmi V (2013) A potent neurotoxic effect of the methanolic extract of the Parazoanthus mediated by NMDA receptors. Pharmacologia 4:132–137 Ramírez-Carreto S, Pérez-García EI, Salazar-García SI, Bernáldez-Sarabia J, Licea-Navarro A, Rudiño-Piñera E, Pérez-Martínez L, Pedraza-Alva G, Rodríguez-Almazán C (2019) Identifica- tion of a pore-forming protein from sea anemone Anthopleura dowii Verrill (1869) venom by mass spectrometry. J Venom Anim Toxins incl Trop Dis 25:1678–9199 Ramkumar S, Arun Sudhagar S, Venkateshvaran K (2012) Bioactivity of venom extracted from the sea anemone Anthopleura asiatica (Cnidaria: Anthozoa): toxicity and histopathological studies. Int J Fish Aquac 4:71–76 Ravindran VS, Kannan L, Venkateshwaran K (2010) Bioactivity of sea anemone proteins: 1. Toxicity and histopathology. Indian J Exptl Biol 47:1225–1232 Reese E, Depenbrock P (2014) Water envenomations and stings. Curr Sports Med Rep 13:126–131 Reimer A (2017) All things jelly fish; science, facts, treatment for sting, and where they are. http:// angelikasworld.org/all-things-jelly-fishsciencefactstreatment-for-stingand-where-they-are/ Remigante A, Costa R, Morabito R, Spada GL, Marino A, Dossena S (2018) Impact of scyphozoan venoms on human health and current first aid options for stings. Toxins 10:133 Resgalla C Jr, Gonçalves VC, Klein AHF (2005) The occurrence of jellyfish stings on the Santa Catarina Coast, southern Brazil. Braz J Oceanogr 53:183–186 328 References

Resgalla C Jr, Rosseto AL, Haddad V Jr (2011) Report of an outbreak of stings caused by Olindias sambaquiensis Muller, 1861 (Cnidaria: hydrozoa) in Southern Brazil. Braz J Oceanogr 59:391–396 Rifkin JF, Fenner PJ, Williamson JAH (1993) First aid treatment of the sting from the hydroid Lytocarpus philippinus: the structure of, and in vitro discharge experiments with its nematocysts. J. Wilderness Med 4:252–260 Rocha J, Peixe L, Gomes NCM, Calado R (2011) Cnidarians as a source of new marine bioactive compounds—an overview of the last decade and future steps for bioprospecting. Mar Drugs 9:1860–1886 Rodríguez AA, Salceda E, Garateix AG, Zaharenko AJ, Peigneur S, López O, Pons T, Richardson M, Díaz M, Hernández Y, Ständker L, Tytgat J, Soto E (2014) A novel sea anemone peptide that inhibits acid-sensing ion channels. Peptides 53:3–12 Rodríguez AA, Garateix A, Salceda E, Peigneur S, Zaharenko J, Pons T, Santos Y, Arreguín R, Ständker L, Forssmann W, Tytgat J, Vega R, Soto E (2018) PhcrTx2, a new crab-paralyzing peptide toxin from the sea anemone Phymanthus crucifer. Toxins 10:72 Rodsuwan U, Thumthanaruk B, Kerdchoechuen O, Laohakunjit N (2016) Functional properties of type A gelatin from jellyfish (Lobonema smithii). Int Food Res J 23:507–514 Rondan J (2018) Prevention, management and treatment; injuries, punctures and incursions of the marine fauna of Guadeloupe. Ph.D. Thesis (For the Pharmacy Doctors), Universite Toulose III Rosenberg P (1978) Toxins: plant, animal and microbial. Pergamon Press, Oxford. 1031 p Russell SFS (1965) Advances in marine biology, vol Volume 3. Academic Press, London & New York Sammarco PW, Coll JC (1988) The chemical ecology of alcyonarian corals (Coelenterata: Octocorallia). Bioorg Mar Chem 2:87–116 Santana ANC, Leite AB, França MSF, França L, Vale OC, Cunha RB, Ricart CAO, Sousa MV, Carvalho KM (1998) Partial sequence and toxic effects of granulitoxin, a neurotoxic peptide from the sea anemone Bunodosoma granulifera. Braz J Med Biol Res 31:1335–1338 Santhanam R, Ramesh S, Shivakumar G (2019) Biology and ecology of pharmaceutical marine cnidarians (series: biology and ecology of pharmaceutical marine life). CRC Press (Taylor & Francis), Boca Raton. 424 p Santhanam R, Srinivasan A (1994) A manual of marine zooplankton. Oxford & IBH Publishing Co. Pvt. Ltd, New Delhi. 160 p Santhanam R, Srinivasan A, Ajmal Khan S (2015) Manual of methods for marine plankton. Astral Publishing Co., Delhi. 228 p Schlesinger A, Zlotkin E, Kramarsky-Winter E, Loya Y (2009) Cnidarian internal stinging mechanism. Proc R Soc B 276:1063–1067 Schmitt C, de Haro L (2013) Clinical marine toxicology: a European perspective for clinical toxicologists and poison centers. Toxins 5:1343–1352 Segura-Puertas L, Avila-Soria G, Sánchez-Rodríguez J, Ramos-Aguilar ME, Burnett JW (2002) Some toxinological aspects of Aurelia aurita (Linné) from the Mexican Caribbean. J Venom Anim Toxins 8:269–282 Sencic L, Macek P (1990) New method for isolation of venom from the sea anemone Actinia cari. Purification and characterization of cytolytic toxins. Comp Biochem Physiol 97B:687–693 Seyedian R, Lee S, Kim J, Yoon W (2007) Cardiovascular effects of Nemopilema nomurai (Scyphozoa: Rhizostomeae) jellyfish venom in rats. Toxicol Lett 167:205–211 Shier WT (1990) Handbook of toxinology. CRC Press, Boca Raton. 872 p Shiomi K, Qian W, Lin X, Shimakura K, Nagashima Y, Ishida M (1997) Novel polypeptide toxins with crab lethality from the sea anemone, Anemonia erythraea. Biochim Biophys Acta 1335:191–198 Shiomi K, Takamiya M, Yamanaka H, Kikuchi T (1986) Physicochemical properties of a lethal hemolysin isolated from the sea anemone Anthopleura japonica. Nihon Suisan Gakkai Shi 52:539–543 References 329

Shryock JC, Bianchi CP (1983) Sea nettle (Chrysaora quinquecirrha) nematocyst venom: mechanism of action on muscle. Toxicon 21:81–95 Simmons BJ, Griffith RD, Falto-Aizpurua LA (2015) Moon jellyfish stings. JAMA Dermatol 151:454–456 Sket D, Drašlar K, Ferlan I, Lebez D (1974) Equinatoxin, a lethal protein from Actinia equina—II. Pathophysiological action. Toxicon 12:63–68 Sorokin Y (1993) Coral reef ecology. Springer-Verlag, Berlin Ständker L, Béress L, Garateix A, Christ T, Ravens U, Salceda E, Soto E, John H, Forssmann WG, Aneiros A (2006) A new toxin from the sea anemone Condylactis gigantea with effect on sodium channel inactivation. Toxicon 48:211–220 Sucharitakul P, Chomdej S, Achalawitkun T, Arsiranant I (2017) Description of Chironex indrasaksajiae sucharitakul sp. nov. (Cnidaria, Cubozoa, Chirodropida): a new species of box jellyfish from the Gulf of Thailand. Phuket Mar Boil Cent Res Bull 74:33–44 Sunahara S, Muramoto K, Tenma K, Kamiya H (1987) Amino acid sequence of two sea anemone toxins from Anthopleura fuscoviridis. Toxicon 25:211–219 Suput D (2011) Interactions of cnidarian toxins with the immune system. Inflamm Allergy Drug Targets 10:429–437 Sutton A (2016) Stinging sea creatures-fireweed. https://seaunseen.com/stinging-sea-creatures-fire weed/. Accessed 11 Jul 2019 Talvinen KA, Nevalainen TJ (2002) Cloning of a novel phospholipase A2 from the cnidarian Adamsia carciniopados. Comp Biochem Physiol B Biochem Mol Biol 132:571–578 Tamanaha RH, Izumi AK (1996) Persistent cutaneous hypersensitivity reaction after a Hawaiian box jellyfish sting (Carybdea alata). J Am Acad Dermatol 36:991–993 Tesseraux I, Gülden M, Schumann G (1989) Effects of toxin isolated from the sea anemone Bolocera tuediae on electrical properties of isolated rat skeletal muscle and cultured myotubes. Toxicon 27:201–210 Tezcan ÖD (2016) Unusual cnidarian envenomations. In: Goffredo S, Dubinsky Z (eds) The cnidaria, past, present and future. Springer, Cham, pp 609–622 Tezcan ÖD, Sarp S (2013) An unusual marine envenomation following a rope contact: a report on nine cases of dermatitis caused by Pennaria disticha. Toxicon 61:125–128 Thangaraj S, Bragadeeswaran S (2012) Assessment of biomedical and pharmacological activities of sea anemones Stichodactyla mertensii and Stichodactyla gigantea from Gulf of Mannar Biosphere Reserve, southeast coast of India. J Venom Anim Toxins Incl Trop Dis 18:53–61 Thomson M, Moritz RL, Simpson RJ, Norton RS (1987) Tenebrosin-a, a new cardiostimulant protein from the Australian sea anemone Actinia tenebrosa. Biochem Int 15:711–718 Tibballs J, Li R, Tibballs HA, Gershwin L, Winkel KD (2012) Australian carybdeid jellyfish causing “Irukandji syndrome”. Toxicon 59:617–625 Tibballs J, Yanagihara AA, Helen C, Turner HC, Winkel K (2011) Immunological and toxinological responses to jellyfish stings. Inflamm Allergy Drug Targets 10:438–446 Tkacheva ES, Leychenko EV, Monastyrnaya MM, Issaeva MP, Zelepuga EA, Anastuk SD, Dmitrenok PS, Kozlovskaya EP (2011) New Actinoporins from sea anemone Heteractis crispa: cloning and functional expression. Biochemistry 76:1131–1139 Turk T (1999) Poisonous and venomous organisms of the Northern Adriatic Sea. Ann Ser Hist Nat 9:159–166 Turk T, Maček P, Šuput D (1995) Inhibition of acetylcholinesterase by a pseudozoanthoxanthin- like compound isolated from the zoanthid Parazoanthus axinellae (O. Schmidt). Toxicon 33:133–142 Uechi G, Toma H, Arakawa T, Sato Y (2005) Biochemical and physiological analyses of a hemolytic toxin isolated from a sea anemone Actineria villosa. Toxicon 45:761–766 Uechi G, Toma H, Arakawa T, Sato Y (2011) Characterization of a novel proteinous toxin from sea anemone Actineria villosa. Protein J 30:422–428 330 References van Losenoord W, Krause J, Nance SP, Frost C (2018) Isolation and characterization of a potassium channel inhibitor isolated from Bunodosoma capensis. Biochem Mol Biol J. https://doi.org/10. 21767/2471-8084-C4-018 Veeruraj A, Arumugam M, Ajithkumar T, Balasubramanian T (2008) Isolation and biological properties of neurotoxin from sea anemone (Stichodactyla mertensii, S. haddoni). J Toxicol 5:1–11 Waggoner BM, Collins A, Smith D (1994) Introduction to the Anthozoa. https://ucmp.berkeley. edu/cnidaria/anthozoa.html. Accessed 11 Jul 2019 Wiles JS, Vick JA, Christensen MK (1974) Toxicological evaluation of palytoxin in several animal species. Toxicon 12:427–433 Wiltshire CJ, Sutherland SK, Fenner PJ, Young AR (2000) Optimization and preliminary characterization of venom isolated from 3 medically important jellyfish: the box (Chironex fleckeri), Irukandji (Carukia barnesii), and blubber (Catostylus mosaicus) jellyfish. Wilderness Environ Med 11:241–250 Williamson JA, Fenner PJ, Burnett JW, Rifkin JF (1996) Venomous and poisonous marine animals: a medical and biological handbook. University of New South Wales Press, Sydney, pp 119–310 Winter KL, Fernando R, Ramasamy S, Seymour JE, Isbister GK, Hodgson WC (2007) The in vitro vascular effects of two chirodropid (Chironex fleckeri and Chiropsella bronzie) venoms. Toxicol Lett 168:13–20 Wittle LW, Scura ED, Middlebrook RE (1974) Stinging coral (Millepora tenera) toxin: a comparison of crude extracts with isolated nematocyst extracts. Toxicon 12:481–482 Yamaguchi Y, Hasegawa Y, Honma T, Nagashima Y, Shiomi K (2010) Screening and cDNA cloning of Kv1 potassium channel toxins in sea anemones. Mar Drugs 8:2893–2905 Yoshimoto CM, Yanagihara AA (2002) Cnidarian (coelenterate) envenomations in Hawai’i improve following heat application. Trans R Soc Trop Med Hyg 96:300–303 Yost GA, O’Brien RD (1978) Isolation of the two components of Condylactis toxin. Arch Biochem Biophys 185:483–487