The Aquatic Biotic Environment and Its Biotoxins

Abstract

The aquatic world is renowned for its enchanting beauty. In some cases, however, hidden perils may lurk behind the alluring beauty, and even some mortal dangers. An analysis of the map of the hydrosphere shows that the central hub for potentially harmful aquatic animals is the great area of the Indian and Pacific Oceans, although aquatic animals and vegetables of less aggressive type are present in all the seas. Of the two types of offense and defense mechanisms possessed by many marine fauna, namely physical and chemical, study of the latter has always been a fascinating sector of marine biology, still to some extent veiled in an aura of mystery. Many animal and vegetable species are equipped with biotoxins, organic products that can be poisonous (harmful when eaten) or venomous (harmful when they enter the bloodstream), and have various different actions and variable pathogenic intensities. These biotoxins can be actively produced, or else derive from the aquatic environment for various reasons. In the latter case the animals are carriers of biotoxins. To date, few biotoxins have been isolated, of variable chemical natures, and with a few exceptions, no specific antidotes have yet been discovered.

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The aquatic world, together with its animal kingdom, is renowned for its enchanting beauty (Fig. 2.1). In particular, the vast tropical coral reefs offer a shimmering, glittering underwater panorama featuring an infinite variety of hues, sometimes clashing but always ultimately harmonising. In some cases, however, these beautiful shapes, elegant movements and profusion of colours seem to go hand in hand with disease and death. This is one of the great paradoxes of the aquatic world.

Fig. 2.1

Hyppocampus guttulatus (sea horse) (Courtesy of Drs. Pablo Helman and Susanna Volpe, “Il quaderno blu”, Provincia di Imperia Ed., 1995)

An analysis of the map of the hydrosphere shows that the centre of the world of potentially harmful aquatic animals is the great area of the Indian and Pacific Oceans, although aquatic animals of less aggressive type are present in all the seas. The defence and/or offence mechanisms of marine fauna can be of two different types, physical or chemical (Table 2.1). Some observations of the latter type have unveiled a fascinating sector of marine biology that is still largely a mystery.

Table 2.1 Aquatic animals and types of lesions they provoke

Aquatic biotoxicology is the science that studies aquatic biological toxins, and as this book focuses above all on the skin damage that can be wrought by poisonous or venomous aquatic creatures, it seems wise to start off with an overall classification of poisonous aquatic animals [1–5].

2.1 Toxic Aquatic Animals

The brief classification of poisonous aquatic animals listed below includes a large number of species living in enormously different geographical areas and habitats [2].

2.1.1 Invertebrates

Invertebrate poisonous aquatic animals, i.e., those with no backbone, can be subdivided into the following groups or phyla.

• 1. Protozoa

  This group includes single-cell planktonic organisms with which man can come in contact when eating molluscs or fish that feed on Dinoflagellates.

• 2. Porifera

  Some sponges produce chemical substances that are highly irritant to the skin.

• 3. Cnidaria (Coelenterata)

  Few species of Coelenterates are poisonous to eat but most of them are venomous.

• 4. Platyhelminthes

  Various species of Platyhelminthes are considered poisonous to eat.

• 5. Annelida

  Some Polychaetae worms are equipped with irritant hairs or spines, while others have venomous glands.

• 6. Mollusca

  Many bivalvular molluscs are transvectors of various toxic substances. The cone shell and the octopus are included in this class of molluscs with a venomous apparatus.

• 7. Arthropoda

  Some species of Asiatic crabs are poisonous to eat. There are also a few species of poisonous aquatic insects, belonging to five different families of bugs that inhabit freshwater.

• 8. Echinodermata

  Some species of sea urchins are poisonous because their eggs are toxic, and so are some sea cucumbers.

2.1.2 Vertebrates

• 1. Poisonous and venomous fishes

  Many fish can cause human bio-intoxication when eaten, due to the presence of toxic substances. This class does not include fish that have been accidentally contaminated by pathogenic bacteria. The largest category is that of ichthysarcotoxic fish, that contain poisonous substances in their muscles, viscera or skin, that obviously cannot be destroyed by heat or gastric juices. The second major category of poisonous fish is that of ichthyocrinotoxic fish, that release toxins through the skin by means of specialised secretory organs. The third category includes the various venomous fish with specialised secretory organs and a wound-producing apparatus, such as spines or teeth.

• 2. Venomous amphibia

  Some amphibians (salamanders, toads, newts) produce very strong poisons.

• 3. Poisonous reptiles

  Some species of sea turtles are considered to become poisonous through eating toxic plants, but the precise source of the poison is unknown. Water snakes make up the most numerous reptile category, and some of these contain very potent poisons.

• 4. Poisonous mammals

  The liver of some whales, polar bears, walruses, seals and sea lions can be toxic.

2.2 The Functions of Biotoxins

Biotoxins, i.e., “poisonous” organic products of bacterial, vegetable or animal origin, are substances that have various different biological actions, of variable severity, when introduced into other organisms. A substance, of animal or vegetable origin, is poisonous if it is harmful to eat (e.g., some mushrooms and some fish are poisonous). Instead, an animal is “venomous” if it produces substances that are harmful when they enter the bloodstream (e.g., the viper and some Coelenterates are venomous, but their secretions are innocuous when eaten). Obviously, the toxic products of a venomous animal can be harmful when injected [5].

As shown above, many species of marine Vertebrates and Invertebrates produce biotoxins. An animal will be described as “poisonous” or “venomous” according to the use it makes of its poison: when it is used as a defence or offence mechanism and to capture prey for food, the animal is said to be “venomous”, or actively toxic. Instead, a “poisonous” or passively toxic animal produces or ingests substances that are harmful when the animal is eaten [5].

There are large volumes of data in the literature on the biotoxins of marine animals [6–17]. Some general notions are reported below, while the toxins inherent to each animal species will be dealt with in the relative chapters.

Most marine animal poisons serve to capture prey for food. However, not all marine animals use toxins just to procure food: microphagic animals feed on live or dead organisms and organic waste floating in the water or mingled with the sand, and therefore filter the water or ingest the sand to obtain the nourishing substances. For this reason, some of these animals may be toxin carriers because they act as filters, and so any toxic substances present in the micro-organisms or in the aquatic environment will accumulate in their organs and make them poisonous to eat.

Instead, macrophagic animals need to use defence and offence mechanisms to capture and immobilize their prey. Hence, while the mammalian salivary glands have only a digestive function, in many Invertebrates and some Vertebrates (snakes) these glands secrete substances that are actively toxic to the prey’s nervous system or other organs. Cephalopod Molluscs, for instance, immobilize their prey with secretions from their posterior salivary glands, which contain both digestive proteolytic enzymes and biotoxins. Snakes also produce many poisons that are injected with their saliva into victims. Coelenterates capture their prey, such as fish, with their tentacles and immobilize them by injecting toxins through the nematocysts. Not all the action mechanisms of these immobilizing neurotoxins are known: some act on the brain centres or ganglial chains, and others on the peripheral nervous system by impeding the conduction or transmission of nerve impulses at the level of the neuromuscular sheath.

Biotoxins may be used purely as defence mechanisms. The scorpionfish (Scorpaena) defends itself from predators thanks to its venomous dorsal spines. The ray (Dasyatis) has a strong, well-developed sting apparatus in the tail which is thrust into the body of the predator. Not only does this organ provoke a painful, lacerating wound, but it also conveys the secretions of the potent poison glands situated at its base.

In short, when they are produced by the salivary glands, biotoxins serve above all to capture prey for food. The biotoxins in the nematocysts of Coelenterates have the same function. Instead, when they are secreted by glands at the base of the spine or radioles, they have a defensive function against other animals. The role of the toxins present in the muscles or ovaries of many marine animals is difficult to ascertain, but what is certain is that owing to these toxins, such animals are poisonous to other animals and man.

2.3 The Biochemistry of Biotoxins

Up to now, the biochemical make-up of only relatively few biotoxins has been identified, for various reasons: it is difficult to obtain sufficient material for extracting and purifying the poisons, while we have little knowledge of the environmental distribution of many pelagic or deep-sea animals, and no suitable means for capturing them.

The biotoxins whose chemical nature is known are of various types: some are simple amino or phenol derivatives with a low molecular weight, or choline esters, or derivatives of steroid or isoquinoline compounds; others are peptides formed by few amino acids or proteins with a high molecular weight.

Generally, a venomous gland produces various compounds with different functions and chemical structures: the nematocysts of the Coelenterates, for example, contain many active substances with high and low molecular weights.

Research on the synthesis and metabolism of biotoxins is still in its infancy. With a few exceptions, no antidotes to the various poisons have yet been discovered, even for those that can cause mortal epidemics, like mytilotoxin and tetrodotoxin.