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4.09 Chemical Defense and Toxins of Lower Terrestrial and Freshwater Animals Konrad Dettner, University of Bayreuth, Bayreuth, Germany

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4.09 Chemical Defense and Toxins of Lower Terrestrial and Freshwater Animals Konrad Dettner, University of Bayreuth, Bayreuth, Germany 4.09 Chemical Defense and Toxins of Lower Terrestrial and Freshwater Animals Konrad Dettner, University of Bayreuth, Bayreuth, Germany ª 2010 Elsevier Ltd. All rights reserved. 4.09.1 Introduction 387 4.09.2 Alveolata 388 4.09.3 Porifera 390 4.09.4 Cnidaria 390 4.09.5 Platyhelminthes (Flatworms) 391 4.09.6 Nemathelminthes: Nematoda 391 4.09.7 Rotatoria (Rotifers) 391 4.09.8 Nemertini 391 4.09.9 Mollusca 392 4.09.10 Annelida: Clitellata: Oligochaeta 393 4.09.11 Annelida: Clitellata: Hirudinea 394 4.09.12 Arthropoda: Onychophora 394 4.09.13 Arthropoda: Tardigrada 395 4.09.14 Arthropoda: Crustacea, Ostracoda 395 4.09.15 Arthropoda: Crustacea, Decapoda 395 4.09.16 Arthropoda: Crustacea, Amphipoda 395 4.09.17 Arthropoda: Crustacea, Isopoda 395 4.09.18 Arthropoda: Chelicerata, Scorpiones 396 4.09.19 Arthropoda: Chelicerata, Pseudoscorpiones 396 4.09.20 Arthropoda: Chelicerata, Acari (Mites) 396 4.09.21 Arthropoda: Chelicerata, Opiliones 398 4.09.22 Arthropoda: Chelicerata, Pedipalpi 400 4.09.23 Arthropoda: Chelicerata, Araneae 401 4.09.24 Arthropoda: Myriapoda: Opisthogoneata (Centipedes) 402 4.09.25 Arthropoda: Myriapoda: Progoneata: Diplopoda (Millipedes) and Symphyla 403 References 407 4.09.1 Introduction Terrestrial and freshwater animals possess various mechanisms for defense against predatory or patho- genic organisms.1,2 In all animals, defensive substances may be present in tissues, the blood (nonglandular secretion), and exocrine eversible or noneversible glands. Occasionally, such compounds are found in regurgitants or enteric discharges and defecations.3 Certainly, all developmental stages from eggs to adults,4 and also from monocellular to multicellular organisms, that is, from protozoans to vertebrates, may be chemically protected. Many of these natural products represent simple, widely distributed chemicals; however, there are also various unique products,5 frequently restricted to special taxa. The glands may represent oozing, spraying, reactor, or tracheal glands.3 It is also of interest to investigate whether animals manufacture their own toxic or distasteful compounds (intrinsic origin) or whether behavior-modifying chemicals are acquired from host plants, other animals, bacteria, or fungi (extrinsic 387 388 Chemical Defense and Toxins of Lower Terrestrial and Freshwater Animals origin). Considerable biosynthetic knowledge is especially available in insects,6 while data from other animals are less available or missing. Usually, defensive compounds may exert their effect via foul smell (repellents) or bad taste (deterrent). Very often, defensive compounds may induce cleaning behavior in theaggressor,givingthepreytimetoescape.Thereareanumberofirritantcompoundsthatmayalso induce pain. Examples include nonspecific toxicants, or hot secretions. Especially, urticating hairs and delivery of venom by injectable means, for example, stings or fangs, are widely observed. Venoms are usually complex aqueous mixtures of proteins (enzymes), peptides, carbohydrates, nucleosides, biogenic amines, amino acids, lipids, and metallic cations. Many of these toxins represent presynaptic and postsynaptic neurotoxins, cytotoxins, myotoxins, and cardiotoxins. These poisons may act immediately or may show delayed effects (e.g., emetics, vesicants). Certain animals may secrete sticky components that harden like glues and incapacitate attackers.3 The chemistry of these sticky, slimy, or resinous fluids is often not well known. This chapter focuses on low molecular defensive compounds, typical products of secondary metabolism; however, it also covers principal data on high-molecular, behavior-modifying chemicals. Taxonomically, this compilation covers all protozoan and metazoan taxa apart from Deuterostomia (especially vertebrates) and Insecta. Allelochemicals of insects and vertebrates are not included as these have been recently reviewed,7,8 and the actual data will be published elsewhere. Whenever possible, actual reviews are cited and updated. Chemical structures of chiral compounds depicted here reflect the relative or absolute configurations of the substances as far as they are known today. Concerning a wide array of organisms, there exist actual surveys of chemical defenses of insects,3,11–15 arthropods,2,3,4–7,9,10–16 or animals in general.13–15 However, until now, many taxonomically lower animal taxa have never been reviewed with respect to chemical defense. Therefore, here such phenomena are cited in selected taxa even if no or scarce chemical data on the relevant natural compounds are available. Various reviews approach venoms and toxins of animals more generally,15–21 and sometimes may include low molecular defensive com- pounds.16 Taxonomic data are especially taken from Dettner and Peters,22 Storch and Welsch,23 Westheide and Rieger,24 and Resh and Carde´.25 Chemicals of extrinsic origin are not dealt with in detail; however, they may be of special interest if they are chemically modified during metabolic processes. 4.09.2 Alveolata Alveolata include the former unicellular Dinoflagellata, Ciliophora (Ciliata), and Apicomplexa (Sporozoa). It is interesting to note that toxic species within unicellular eukaryotes seem to be restricted to representatives of Alveolata. Among 2500 species of Dinoflagellata, several mostly photosynthetic and marine species produce or accumulate toxins.26 Only representatives of the freshwater and marine genus Gymnodinium are known to 27 produce the pentacyclic imine gymnodimine (1), which is moderately toxic (LD50: intraperitoneal injection, mouse, 96 mg kgÀ1). Some heterotrich ciliates possess specialized exocytotic organelles, the extrusomes. Upon molestation, these structures may discharge material to the cell surface. Especially in ciliates, there are haptocysts (with toxic enzymes), mucocysts (with a protective coat), trichocysts (spindle-shaped bodies with paracrystalline matrix), and toxicysts (tubular structures).28 Recently, it was discovered that the blue and red pigments stentorin (2) and blepharismin (3), two polyketides from the exocytotic organelles of Stentor and Blepharisma, primarily act as chemical defense of these Ciliophora against small predators.29 The same function was ascribed to climacostol (4, 5-(Z)-non-2-enylresorcinol) and the two congeners of climacostol (5, 5-(Z,Z)-undeca-2,5-dienylresorcinol; 6, 5-(Z,Z,Z)-undeca-2,5,8-trienylresorcinol), three colorless lipids isolated from the heterotrich ciliate Climacostomum.30 In addition, spirostomin, spiro[(2.5-dimethyl-5,6,7,8-tetrahydronaphthalene-1,4-dione)-8,69-(pyrane-29,59- dione)], was identified from the ciliate Spirostomum teres.31 It exhibits toxic activities against predatory ciliates. As shown by bioassays, the karyorelictid ciliate Loxodes striatus may release toxin-containing yellow-brown extrusomes, which repel predators such as Dileptus (Ciliata) and Stenostomum (Turbellaria).32 Other high molecular toxins were recorded from the Apicomplexa (Sporozoa). A protein–hyaluronic acid complex (toxotoxin) was described from peritoneal exudates of mice, which is probably produced by hosts in OH O OH OH O OH H OH O O HO O HO OH OH HO HO OH OH HO N OH [1] [2][3] OH O OH OH O OH HO [4] OH OH HO HO [5] [6] 390 Chemical Defense and Toxins of Lower Terrestrial and Freshwater Animals response to coccid infections.33 Moreover, there are known toxic Toxoplasma lysates, such as toxoplasmine, extracts from the cysts of Sarcocystis (Sarcocystin), or an Eimeria toxin.34 A further toxofactor, a glycoprotein (molecular mass (MM) 50 000–100 000), was found to be associated with Toxoplasma gondii.35 [8] HOOC N [9] [13] HOOC N [10] HOOC CO OH HN O O O HO S [11] HOOC OH O O OH [12] HOOC [7] 4.09.3 Porifera The sessile sponges (10 000 species), especially marine species36 and also dry powders of freshwater species,37 may contain a large array of bioactive molecules and may be even used as pharmaceuticals. Also freshwater species of the family Spongillidae contain more than 100 novel unusual and rare fatty acids, lipids, and sterols.38 From the freshwater species Ephydatia syriaca, syriacin (7) was isolated. It is a novel unusual sulfated ceramide glycoside containing a branched long-chain fatty acid, that is, (all Z)-34S-methylhexatriaconta-5,9,12,15,18,21- hexaenoic acid.39 Syriacin showed a distinct antifeeding activity against goldfish. Other freshwater species of the genera Ephydatia, Nudospongilla, and Cortispongilla produce multibranched polyunsaturated and long-chain fatty acids (8–12) that are active against Gram-positive bacteria and have been proved to be toxic against the shrimp Artemia salina.40 Among these compounds, 9 shows an unusual carbon skeleton as the 6,9-methyl branching includes two unsubstituted carbons, which is not in line with a typical biosynthetic scheme involving acetate and propanoate. Finally, a Lubomirskia species from the Lake Baikal and its symbiotic dinoflagellates, which are related to Gymnodinium sanguineum (see gymnodimine (1)), contain the polyether toxin okadaic acid. In the sponge, this strong protein phosphatase 2A inhibitor is present in the free form as well as in a protein- bound state. The authors suppose that the toxin may contribute to the cold resistance of the sponge.41 4.09.4 Cnidaria Just as Porifera, the sessile, predatory, and often soft-bodied Cnidaria (9200 species) depend on offensive and defensive allomones for prey capture and survival. This is also true for the small group of freshwater species belonging to Hydrina (Capitata). The nematocyst venom of Hydra vulgaris has been reported
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