The Fauna Europaea is a database of the scientific names and distribution of all living, currently known multicellular European land and freshwater animal species assembled by a large network of experts using advanced electronic tools for data collation and validation routines.

The 'Helminths (animal parasitic)' is one of the 58 major Fauna Europaea taxonomic groups, covering 3,986 species. The data were acquired and checked by a network of 19 specialists (Tables 1, 2).

 

HELMITNTHS

The animal parasitic helminths (‘parasitic worms’) dealt with in this section include members of three phyla, the Acanthocephala (‘thorny-headed worms’ or 'spiny-headed worms'), Platyhelminthes (‘flatworms’) and Nematoda (‘roundworms’); these are usually referred to as acanthocephalans, platyhelminths and nematodes, respectively. Parasitic worms are usually parasitic at the adult stage, but many are also parasitic as larvae. Many have complex life-cycles involving the ‘definitive’ or ‘final’ host (usually a vertebrate), which harbours the adult stage, and one or more ‘intermediate hosts’ (invertebrate or vertebrate), which harbour the larval stage(s). Others have a direct life-cycle, where the definitive host is infected directly via an egg or a larval stage. Such larval stages are often encysted and survive in this state for long periods. Transmission of the parasite to the definitive host is often by ingestion with its food, or via the direct penetration by a larval stage. In nature, it is the usual condition for animals to be parasitized, so they have evolved to accommodate certain levels of infection. However, in cases where animals are kept or occur in unnaturally high concentrations, e.g. in the cases of farming, aquaculture or even man in villages or urban situations, parasite populations can build, causing them to become pathogenic. However, there are many factors, such as stress, which can cause a reduced resistance to parasites.

The classification and identification of parasitic worms have been based mainly on morphological features, although other factors, such as the host, distribution, site and life-cycle, may also be taken into consideration. In recent years, classifications based on molecular findings, which are thought to approximate closer to a true phylogenetic system, have been introduced. However, their use causes problems in identification, as classifications based on molecules and morphology are rarely totally concordant. Using a molecular classification has the disadvantage that accepted groups may not be recognised, or at least not easily recognised, using morphological criteria. Furthermore, molecular classifications are virtually always based on only an extremely small fraction of the number of taxa and individuals within the group, and consequently many taxa may be left stranded as ‘incertae sedis’. Therefore, although molecular evidence is considered in some recent classifications, taxonomic arrangements still tend to be based mainly on morphological and other biological criteria.

The ACANTHOCEPHALA is a relatively small group of about 1,200 species. Acanthocephalans (Fig. 1) occur as intestinal parasites of a wide range of vertebrates at the adult stage, but are absent from elasmobranch fishes, and are especially prevalent in freshwater teleosts. These parasites are readily recognisable by the possession of a single large, eversible, armed proboscis. They attach using their proboscis, which penetrates the host’s intestinal wall, and resemble tapeworms in that they lack a gut and absorb nutrients from the host’s intestine through their body wall. They are dioecious and have a body-cavity which contains little but their reproductive organs. All acanthocephalans utilise arthropods as intermediate hosts (often crustaceans in the case of species parasitizing aquatic hosts and insects in cases where terrestrial mammals and birds act as final hosts), within which two larval stages occur. The second larval stage, the cystacanth, is an encysted resting stage which normally infects the vertebrate host when the arthropod host is eaten. In some cases, especially those species parasitizing piscivorous mammals and birds, a vertebrate may act as a second intermediate host in which no development occurs (a paratenic host).

In recent classifications (Monks and Richardson 2011; Amin 2013), four (three large and one small) classes are recognised. Useful taxonomic criteria at higher levels include the arrangement of lacunar canals in the syncytial body-wall, the arrangement of cement glands in the males and the nature of large nuclei in the body-wall. At lower taxonomic levels, the number and arrangement of hooks on the proboscis are the major diagnostic features. In the future, molecular studies, such as that of Weber et al. (2013), should help clarify the relationships between the different groups.

The PLATYHELMINTHES (flatworms) include both free-living and parasitic groups. They are bilaterally symmetrical, lack a body cavity, are composed of three main cell layers, usually lack an anus and are usually hermaphroditic. The free-living groups, referred to as the Turbellaria, are dealt with elsewhere, but do include a small number of parasitic or commensal forms. Parasitic platyhelminths form a group called the Neodermata, which comprises three distinct, divergent classes, which have in common a specialised syncytial body-covering, the tegument or neodermis, derived from mesodermal cells. The three classes are the Monogenea, the Trematoda (‘flukes’) and the Cestoda (‘tapeworms’). These groups can be so plastic in terms of their morphology and life-history that there are usually exceptions to every rule.

The Monogenea (also referred to as the Monogenoidea by a small number of workers, but use of this name should be avoided for several reasons, a major one being that it terminates in a superfamily suffix) are a group of about 6,000-7,000 species which are mainly ectoparasitic on fishes, especially on the gills and skin, and occasionally other aquatic organisms, such as amphibians. A small number of species also occur as endoparasites. The majority of monogenean species (Fig. 2) are highly host-specific, usually being restricted to a single host species with which they have co-evolved. A direct life-cycle using a ciliated larva for transmission is usual. However, gyrodactylids are unusual in that they are viviparous, and each worm gives birth to a fully-developed young worm which may have a third generation developing within it (polyembryony); thus their population size can increase very rapidly. In freshwater, the monogenean fauna is dominated by two huge genera, Dactylogyrus and Gyrodactylus, with 900+ and 400+ nominal species, respectively (Gibson et al. 1996; Harris et al. 2004). It is quite common to find more than one species of the same genus on the same host. Generally, monogeneans do little harm to their hosts, but some species, especially some gyrodactylids, can cause mass mortalities in fish-farms and/or situations where the parasite is introduced into an immunologically naive host population.

Monogeneans are generally distinguished by features of their posterior attachment organ (haptor), which is normally armed with attachment clamps and/or anchors and hooks, and in some cases the structure of the sclerotised hardparts of the male and female reproductive systems is also important. Such differences between congeneric species can be very subtle. Classifications vary, but those forms where the haptor is typically armed with clamps (or suckers) and minute (vestigial) hooks are referred to the subclass Polyopisthocotylea (or Oligonchoinea + Polystomatoinea), and those armed with hooks only (some large) belong to the subclass Monopisthocotylea (or Polyonchoinea). Most polyopisthocotyleans live on the gills and feed on blood, whereas most monopisthocotyleans live on the skin or gills and tend to feed on skin and/or mucus. Recent molecular work has suggested that these two groups are independent and that the Monogenea may not be monophyletic (Perkins et al. 2010). At lower levels, morphologically-based classifications, such as that of Boeger and Kritsky (1993), do not always agree with those based on molecular data (e.g. Šimková et al. 2006; Perkins et al. 2010), but some on-line data-bases (e.g. MonoDB (http://www.monodb.org/) have the potential and adaptability to develop a more integrated and useful system.

The Trematoda is a large class of 15,000-20,000 species which utilise all of the major vertebrate groups as hosts. Most trematodes (flukes) are endoparasitic as adults and live in the alimentary canal, but the group is extremely adaptable in terms of site, with different species occurring in most major body cavities and organs, and a very small number being ectoparasitic. One distinctive feature of virtually all trematodes is the involvement of molluscs in their life-history. There are two subclasses, the Aspidogastrea and the Digenea.

The Aspidogastrea is a small, disparate group of fewer than 100 species, whose members occur as gut parasites of molluscs, fishes and turtles. Those in molluscs have a direct life-cycle, whereas those with vertebrate hosts, where the complete life-cycle is known, use molluscs as primary hosts, with transmission by ingestion. They generally have a relatively low level of host-specificity. There are four families, all of which possess either a large, subdivided ventral disc or a row of suckers; only one family, the Aspidogastridae, occurs in freshwater, whereas the other three families are marine. A recent key to the genera can be found in Rohde (2002).

The Digenea is an enormous group of more than 2,500 nominal genera (Gibson 2002). Virtually all use molluscs as primary hosts and the majority occur as sexual adults in vertebrates (all groups), but they are especially prevalent in fishes. Digeneans (Fig. 3) are characterised by having multiple generations (usually three) within their life-cycle – two asexual generations mature in the mollusc host and one sexual generation within a vertebrate host. The first generation, termed the mother-sporocyst, is derived from a ciliated larva, the miracidium, which develops within the egg and infects the mollusc host. The mother-sporocyst produces a second parthenogenetic generation internally, termed a daughter-sporocyst or redia, depending on its morphology. This second generation normally produces a large number of tailed, larval forms of the third, sexual, generation, called cercariae, which are free-living. Transmission to the next host is usually by cercarial penetration or by the ingestion of cercariae. In most cases the cercaria encysts within the tissues of a second (or intermediate) host, which may be an invertebrate or a vertebrate, as a resting stage, the metacercaria. This stage remains within this host until it is eaten by the final host, normally a vertebrate, within which the sexually mature, egg-laying adult develops.

Digeneans are thought to generally exhibit a high level of host-specificity to the mollusc host, a low level to any intermediate host and a variable level to the final host. The form of the life-cycle can be extremely plastic in the different groups; for example, in some the cercaria can encyst on vegetation and the herbivorous final host acquires the parasite in its diet, and, in others, the life-cycle is telescoped via the parasite maturing in a host that at one time during its evolution represented an intermediate host, or is extended by the addition of another vertebrate host via the ingestion of a host that was once the final host. With regard to their morphology, digeneans are even more diverse. Although the standard pattern is for a species to have a sucker at the anterior end and another on the ventral surface, some groups have one sucker and others none at all. Some have a body form which is totally unrecognisable as a digenean to a non-specialist. Other somewhat rare variations in structure are found in groups which have an intestine with an anus or ani, and others have no gut at all. There are rare dioecious forms, forms with the entire life-cycle in one and the same host and forms which live on the gills, in the vascular system or under fish scales. Classifications vary, but recent opinion indicates the presence of only two or three orders. Although there are recent molecular phylogenies (e.g. Olson et al. 2003), the most useful identification aids to the generic level are the three volumes of the ‘Keys to the Trematoda‘ (Gibson et al. 2002; Jones et al. 2005; Bray et al. 2008).

The Cestoda (tapeworms) is a relatively large (c. 8,000 species) and diverse group of parasites, the majority of which are found in the intestine of vertebrates (all groups). Like the acanthocephalans, they lack an alimentary canal and absorb their nutrients through their surface layer (tegument), which bears a dense covering of armed, villus-like structures (microtriches) that greatly increase its surface area and represent the main site for nutrient absorption. Tapeworms (Fig. 4) are also unusual in that the majority are long, tape-like and segmented, with one, or occasionally two, complete sets of reproductive organs in each segment. New segments (proglottids) are formed in the neck region behind the head (scolex); these develop and mature as they pass down the body (strobila) and old, ‘gravid’ segments containing eggs are lost terminally. A small number of basal forms that parasitise fishes (occasionally invertebrates) lack segmentation and possess only one or multiple sets of reproductive organs. Tapeworms vary in size from just a few millimetres to many metres in length. Since most adult tapeworms absorb nutrients though their tegument, they tend to do little physical damage to their host, except perhaps at the point of attachment, but they do extract valuable resources from the intestine and can cause bowel obstruction in the case of heavy infections. These worms do not roam freely in the intestine but attach to the wall of the intestine.

Cestodes generally have a life-cycle involving one or two intermediate hosts. Since adult cestodes are intestinal parasites of vertebrates, the eggs or gravid segments containing eggs pass out with the faeces. In those groups prevalent in terrestrial vertebrates, if the eggs are eaten by a suitable intermediate host, which may be a terrestrial invertebrate (commonly an arthropod) or a vertebrate, they hatch to release a hexacanth (six-hooked) larva, called an onchosphere. In the case of those groups more prevalent in fishes or other aquatic vertebrates, the eggs hatch in water to release a ciliated, motile hexacanth, called a coracidium, which is eaten by an aquatic arthropod intermediate host, such as a copepod. In the intermediate host, the hexacanth usually penetrates the gut wall and develops in the body-cavity into a procercoid. It then develops further, either in the same host or, in cases where the first host is eaten, in a second intermediate host, into a resting, normally encysted, stage, which takes on a variety of names, depending upon its form, e.g. cysticercus, cysticercoids or plerocercoid (Chervy 2002). The definitive host acquires the parasite when it feeds on the intermediate host harbouring the encysted stage.

There are marked differences in the form of the attachment organ on the scolex, which form the main criteria for distinguishing the numerous (c. 15) orders of the group. Other important characters include the shape of the segments and the arrangement and form of the reproductive system(s) within the segments, e.g. the position of the genital pore, the nature of the vitellarium, the size of the cirrus-sac, the shape of the ovary and the nature of the uterus. Some of these features are also used to distinguish genera. At the specific level, the number and morphometrics of the hooks, which commonly form the armature of the scolex, are useful. The functional classification of the group is still based on morphology, but, although the basic arrangement is rather stable, molecular data indicate that some changes are needed. The ‘Keys to the Cestode Parasites of Vertebrates’ (Khalil et al. 1994) provides keys down the generic level, and a molecular classification was given by Olson et al. (2001), with updates by Waeschenbach et al. (2007) and Waeschenbach et al. (2012). Recent work (Kuchta et al. 2008a; Kuchta et al. 2008b) has shown that one of the major and important orders (the Pseudophyllidea) is not monophyletic – this has been replaced by two new orders (the Bothriocephalidea and the Diphyllobothriidea). In addition, a large order of shark parasites, the Tetraphyllidea, has been shown by molecular studies to be paraphyletic. The dismemberment of this taxon is now underway.

The phylum NEMATODA is probably the most abundant and widespread animal group, often occurring in huge numbers in environments ranging from hot springs to polar regions. In addition to free-living marine and freshwater forms, there are free-living forms in the soil and parasitic forms in both animals and plants. At least 30,000 species are known, but this is estimated to be only a very small fraction of those that exist. Nematodes (Fig. 5) are symmetrically bilateral, unsegmented, normally dioecious worms which are usually filiform in shape. Their main features include a body-cavity with a high hydrostatic pressure, a straight digestive tract with an anteriorly terminal mouth and posteriorly subterminal anus, no circulatory system, a simple excretory system and a body wall consisting of an outer layer of cuticle and an inner layer of longitudinal muscles. Those parasitic in animals occur in virtually all invertebrate and vertebrate groups. All nematodes have five life-history stages, four larval and one adult, which are separated by a moult of the cuticle. It is common for the first one or two moults to occur within the egg. The free-living and plant-parasitic members of the group are dealt with elsewhere.

The phylum is divided into two classes, the Adenophorea and the Secernentea, both of which have evolved parasitic members, although the majority of animal parasites belong to the latter group. Major differences between the groups reflect the presence and absence of small sensory structures (phasmids) on the tail and the nature of the excretory system. There is also a fundamental biological difference in the parasitic members, since in adenophoreans the first-stage larva is infective to the definitive (final) host, whereas in the Secernentea it is the third-stage larva.

The life-cycles of parasitic forms may be direct or indirect. Direct life-cycles may involve the ingestion of eggs or larvae with food or, in some cases, the direct penetration of larvae through the skin. Indirect life-cycles usually utilise invertebrate intermediate hosts, but sometimes vertebrates (or larger invertebrates) may act as intermediate or paratenic hosts. Such larvae usually occur, often encysted, in the tissues of intermediate hosts. The majority of nematodes parasitic in vertebrates occur in the alimentary canal; those in other parts of the body often require the migration of larvae through the body to reach these sites. Some groups with a direct life-cycle also have a larval migration from the gut and into the tissues and back to the gut; this represents the vestige of an indirect life-cycle from its evolutionary past. Whichever mode of transmission is utilised, the chance of an egg or larva developing into an adult worm is very small, but this may be compensated for by a huge output of eggs, which in some cases reaches as high as 200,000 per day from a single female worm.

Pathogenicity in the definitive host varies considerably, usually being dependent upon the size of the infection. Those, such as hookworms, which are heavily armed with teeth or other sclerotised mouthparts and browse upon the gut wall, can cause considerable damage. Similarly, forms which migrate around the body, both as adults in the tissues and as larvae (the latter termed a larva migrans), can cause serious problems, especially if they reach sensitive regions such as the brain, liver or eyes.

Features used for identification vary from group to group, but at higher taxonomic levels, the nature of the oesophagus, the form of the head (presence and number of lips, teeth, etc.) and the form of the male tail are usually important. At the specific level, details of the male tail, such as the arrangement of caudal papillae (sensory structures used during copulation) and the length and shape of the spicule or spicules (sclerotised copulatory aids) are important. In most cases, males carry more taxonomically useful information than females, such that the latter are often unidentifiable at the specific level. The most used classification of the nematodes based on morphology is that of ‘Keys to the Nematode Parasites of Vertebrates’, published as a series of 10 booklets between 1974 and 1983. This has recently been re-issued as a single volume (Anderson et al. 2009) and updated by Gibbons (2010). A similar key to the nematode parasites of invertebrates was produced by Poinar (1977). These volumes include keys to the generic level. There are also molecular versions of the classifications of the entire phylum (e.g. Meldal et al. 2007) and of various subgroups (e.g. Nadler and Hudspeth 2000).

Currently living animals in stable populations, largely excluding (1) rare/irregular immigrants, intruder or invader species, (2) accidental or deliberate releases of exotic (pet) species, (3) domesticated animals, (4) foreign species imported and released for bio-control or (5) foreign species largely confined to hothouses.

Other