Cestoda

(Tapeworms)

Phylum Platyhelminthes

Class Cestoda

Number of families 72

Thumbnail description
Internal parasitic flatworms lacking a gut during all stages of their development; adults parasitic in vertebrates, larvae in invertebrate and vertebrate hosts

Evolution and systematics

The class Cestoda encompasses about 5,100–5,200 species, 680 genera, and 72 families. During 1992–2002, annually 30–40 newly discovered species have been added, mostly recorded from tropical habitats (terrestrial and freshwater) or from marine fishes (especially from sharks and rays).

There is no generally accepted concept on the classification of the tapeworms. As of 1999–2002, the validity of the following 15 orders is widely recognized:

1. Gyrocotylidea. In holocephalan fishes (Chimaeriformes). Intermediate hosts unknown (life cycle without intermediate hosts was hypothesized). One family (Gyrocotylidae), one to two genera, and about 10 species.
2. Amphilinidea. In freshwater and marine fishes and freshwater turtles. Intermediate hosts: crustaceans. Two families (Amphilinidae and Schizochoeridae), six genera, and about eight species.
3. Caryophyllidea. In siluriform and cypriniform freshwater fishes. Intermediate hosts: tubificid annelids. Four families (Balanotaeniidae, Lytocestidae, Caryophyllaeidae, and Capingentidae), about 45 genera, and 140 species
4. Pseudophyllidea. Mostly in freshwater and marine teleost fishes, also in amphibians, reptiles, birds, and mammals. Intermediate hosts: crustaceans (first or only), usually fishes, rarely other vertebrates (second). Six families (Bothriocephalidae, Philobythiidae, Echinophallidae, Triaenophoridae, Diphyllobothriidae, and Cephalochlamydidae), about 60 genera, and 280 species.
5. Spathebothriidea. In chondrostean and teleost fishes; marine and fresh water. Intermediate hosts: amphipod crustaceans. Two families (Spathebothriidae and Acrobothriidae), five genera, and six to seven species.
6. Haplobothriidea. In relict freshwater fishes (Amiiformes). Intermediate hosts: copepod crustaceans (first) and fishes (second). One family (Haplobothriidae), one genus, and two species.
7. Diphyllidea. In elasmobranch fishes. Intermediate hosts unknown. Three families (Echinobothriidae, Macrobothriidae, and Ditrachybothriidae), three genera, and about 35 species.
8. Trypanorhyncha. In elasmobranch fishes. Intermediate hosts: copepod crustaceans, possibly also other marine invertebrates (first), marine teleost fishes (second). Nineteen families (Tentaculariidae, Paranybeliniidae, Hepatoxylidae, Sphyriocephalidae, Tetrarhynchobothriidae, Eutetrarhynchidae, Gilquiniidae, Shirleyrhynchidae, Otobothriidae, Rhinoptericolidae, Pterobothriidae, Grillotiidae, Molicolidae, Lacistorhynchidae, Dasyrhynchidae, Hornelliellidae, Mustelicolidae, Gymnorhynchidae, and Mixodigmatidae), about 50 genera, and 300–350 species.
9. Tetraphyllidea. In elasmobranch and holocephalan fishes. First intermediate hosts unknown, larvae found in marine teleost fishes (possible second intermediate or paratenic hosts). Seven families (Cathetocephalidae, Disculicipitidae, Prosobothriidae, Dioecotaeniidae, Onchobothriidae, Phyllobothriidae, and Chimaerocestidae), about 60 genera, and 800 species.
10. Litobothriidea. In lamniform sharks. Intermediate hosts unknown. One family (Litobothriidae), one genus, and eight species.
11. Lecanicephalidea. In elasmobranch fishes. Intermediate hosts unknown. Four families (Polypocephalidae, Anteroporidae, Tetragonocephalidae, and Lecanicephalidae), about 12 genera, and 45 species.
12. Proteocephalidea. Mostly in freshwater fishes, also in amphibians and reptiles connected with freshwater habitats. Thaumasioscolex didelphidis, described in 2001 from opossums in Mexico, is the only species of this order known from a mammalian host. Intermediate hosts: copepods (only or first), fishes and amphibians (second). Two families (Proteocephalidae and Monticelliidae), about 50 genera, and 320 species.
13. Nippotaeniidea. In freshwater teleost fishes. Intermediate hosts: copepod crustaceans. One family (Nippotaeniidae), two genera, and about six species.
14. Tetrabothriidea. In marine birds and mammals. Intermediate hosts unknown. One family (Tetrabothriidae), six genera, and about 50 species.
15. Cyclophyllidea. In tetrapods: mostly in birds and mammals, some species in reptiles and amphibians. Intermediate hosts: arthropods, annelids, mollusks or mammals (only or first), fishes, amphibians, reptiles, birds or mammals (second). Eighteen families (Mesocestoididae, Anoplocephalidae, Linstowiidae, Inermicapsiferidae, Thysanosomatidae, Catenotaeniidae, Nematotaeniidae, Progynotaeniidae, Acoleidae, Dioecocestidae, Amabiliidae, Davaineidae, Dilepididae, Dipylidiidae, Hymenolepididae, Paruterinidae, Metadilepididae, and Taeniidae), about 380 genera, and 3,100 species.

The phylogenetic relationships and the classification of the tapeworms are often disputed. According to the traditional views, the tapeworms have been considered the most primitive group among the parasitic flatworms. Two subclasses have been recognized within this class: Cestodaria, including the monozoic orders Gyrocotylidea and Amphilinidea, and Eucestoda, comprising remaining orders (mostly polyzoic but also monozoic). Some authorities consider Amphilinidea and Gyrocotylidea as distinct classes within the phylum Platyhelminthes (as Amphilinida and Gyrocotylida, respectively). Sometimes the order Caryophyllidea (encompassing monozoic worms) is placed out of the Eucestoda and believed to be close to the amphilinideans and gyrocotylideans.

However, as of 1999–2002, mostly as a result of extensive phylogenetic studies based on morphology (including ultrastructure) and molecular data, a wide consensus has been achieved on several points. The Cestoda, comprising Gyrocotylidea, Amphilinidea, and Eucestoda, are believed to form a monophyletic and highly derived flatworm group. One of the major characters supporting their monophyly is the lack of an intestine in all stages of their development. Some further characters, mostly connected with ultrastructural peculiarities of the osmoregulatory system and the tissue covering the body, also confirm their origin from a common ancestor.

The tapeworms, together with the monogeneans and the trematodes, belong to a monophyletic taxon named Neodermata (i.e., "having new skin"). This name reflects the fact that the ciliated epidermis of the larvae is replaced during the metamorphosis by a peculiar syncytial tissue (tegument or neodermis) occurring in adult worms. Main functions of the tegument are protective (against host's immune reactions and enzymes) and digestive (as a major site of absorption, metabolic transformations, and transport of nutrients). The tegument consists of a surface syncytial layer (distal cytoplasm) connected by cytoplasmic bridges with cell bodies (cytons). The cytons, containing nuclei and possessing powerful secretory apparatus, are situated deeply beneath the superficial muscle layers; therefore, they are well protected against host's reactions. Their secretions permanently renovate the distal cytoplasm, which acts as a contact zone between the parasite body and the host's tissues and fluids. Thus, the tegument is an important adaptation for parasitic life (all the adult neodermatans are parasitic). In addition, a range of further characters also is important for defining the Neodermata as a monophyletic group. These are some peculiarities in the structure of the locomotory cilia and the sensory receptors and common patterns of some processes in the course of the spermatogenesis and the formation of the excretory organs.

The monogeneans are believed to be the closest relatives of the tapeworms. The two groups are included in the superior taxon Cercomeromorphae. Their phylogenetic relationships are mostly supported by the presence of set of hooks in the posterior end of the body. In the Eucestoda, these hooks occur in larvae (six embryonic hooks), rarely in both larvae and adults (10 hooks in Gyrocotylidea and Amphilinidea). In eucestode larvae, the embryonic hooks are often situated in a distinct portion of the body (cercomer), which is usually delimited by a constriction from the anterior part of the body. As a rule, the cercomer together with embryonic hooks is detached in the course of the development of the eucestode larvae before its transmission to the final host. In contrast, the caudal hooks of the monogenean larvae are persistent in adult worms as important elements of their attachment apparatus (haptor). The belief that the eucestode cercomer is homologous to the monogenean haptor (not explicitly supported by recent studies) gave the name of the Cercomeromorphae.

Within the Cestoda, the Gyrocotylidea have a basal position to the branch containing the remaining taxa (Amphilinidea plus eucestode orders). Among the Eucestoda, the monozoic order Caryophyllidea is considered basal to the remaining orders. Among the polyzoic orders, these having as a rule four suckers or bothridia on the scolex (known as tetrafossate, e.g., Tetraphyllidea, Proteocephalidea, and Cyclophyllidea) are considered more derived than those having two bothria or bothridia (difossate, e.g., Pseudophyllidea and Diphyllidea).

The monophyly of the Neodermata and the Cercomeromorphae as well as the phylogenetic interrelations within the Cestoda also are well supported by comparisons of their gene sequences.

There are no fossil records of cestodes. However, the phylogenetic studies and the analyses of the evolutionary associations with hosts suggest a long period of the eucestode-vertebrate coevolution, perhaps since the Devonian (before 350–420 million years).

Physical characteristics

The body of the tapeworms is usually dorso-ventrally flattened, narrow, and highly elongate. It resembles a tape, which may explain the etymology of both common and scientific names of the class ("cestus" in Latin means belt, girdle, or ribbon). The size range varies very much: from 0.02 in (0.6 mm) length of the cyclophyllidean Mathevolepis petrotschenkoi (parasite of shrews) to 98 ft (30 m) length of the pseudophyllidean Hexagonoporus physeteris (from the sperm whale). As a rule, tapeworms are whitish because as internal parasites living in darkness they do not possess any pigments.

Typically, the body of tapeworms consists of three distinct regions: scolex (plural scoleces), neck, and strobila (plural strobila).

The scolex (sometimes referred to as "head") is the anterior end of the body. Its major function is the attachment of the parasite to the wall of the intestine. By this reason, it may bear spines, hooks, glands releasing adhesive secretions, grooves, suckers, tentacles, etc., or various combinations of these depending on the ordinal or family affiliation of the worm. The suckers are the most widespread attachment organs (e.g., in Cyclophyllidea, Proteocephalidea, Lecanicephalidea, and in some Tetraphyllidea). They are usually cup shaped, with powerful muscular walls, four in number, two dorsal and two ventral. The bothridium (plural bothridia) is an ear-shaped muscular outgrowth projecting sharply from the scolex and often possessing leaflike mobile margins. The bothridia are usually four in number; they might be sessile or situated at the end of elongate stems connecting them with the scolex. Bothridia occur in several orders (Trypanorhyncha,

Diphyllidea, Tetraphyllidea, and Tetrabothriidea). The bothria (singular bothrium) are simple longitudinal grooves on the scolex, two in number (e.g., in Pseudophyllidea).

The scoleces of the worms of many orders are characterized by the presence of an apical organ consisting mostly of muscular and (or) glandular tissue. In some tetraphyllideans, this organ is represented by a well-developed gland at the apex of the scolex. In the majority of the proteocephalideans, the apical organ has more or less a structure identical to that of the suckers (often referred to as "apical sucker"); however, there are species of this order with an apical organ transformed into a sac filled up of glandular tissue. An immense variability of the structure of the apical organ can be seen in the Cyclophyllidea, where it is usually marked as a rostellum. It is protrusible, often dome-shaped, and in the most common case provided by one or two rows of hooks. In some families, the rostellum can be withdrawn in a special muscular pouch (rostellar sac). The protruded rostellum penetrates deeply into the intestinal wall of the host, anchoring there by the crown of hooks situated on its top. In addition, some cyclophyllideans may have accessory circles of spines or strongly

developed glands associated with the rostellum, also facilitating the reliable attachment to the intestinal wall.

The neck is the region of the body just posterior to the scolex. It is usually short. This is a zone of proliferation, containing numerous stem cells. The latter are responsible for giving rise of the strobila.

The strobila is posterior to the neck. It consists of proglottides arranged in a linear series. The proglottis is a distinct portion of the body containing a set of reproductive organs. The stobila may contain from few (two in Mathevolepis petrotschenkoi), several dozens (in the majority of tapeworms), or numerous (more than thousand in Taenia saginata) proglottides. Each proglottis starts its development at the neck, as a result of the division of the stem cells. Typically, the formation of proglottids one by one at the neck is a permanent process lasting the whole life of the tapeworm in the final host. Just posterior to the neck, the proglottides are short and narrow, containing undifferentiated cells (juvenile proglottides). With the appearance of a new proglottis at the neck, already formed proglottides are pushed in posterior direction, which coincides with their growth and the gradual development of the reproductive organs in them. After the juvenile proglottides, each strobila typically contains the following types of proglottides (from anterior to posterior direction):

• Premature proglottides, with primordia of genital organs only.
• Mature proglottides, with developed and functioning male and female genital systems (almost all tapeworms are hermaphroditic).
• Postmature proglottides, in which the uteri are filled of developing eggs and gonads gradually degenerate.
• Gravid proglottides, containing uteri with ripe eggs.

As a rule, the gravid proglottides having terminal position in the strobila detach after completing their development. They pass to the environment with the host's feces or disintegrate along their route and only eggs are released.

Formation of proglottides occurs in 11 of the orders listed above. However, the members of the orders Gyrocotylidea, Amphilinidea, and Caryophyllidea have only a single set of genital organs per body. Consequently, they have no proglottides. The Spathebothriidea exhibits an intermediate pattern of body organization: an internal multiplication of reproductive organs down the strobila occurs but no distinct proglottides are formed.

In the past, an interpretation of the body organization of the tapeworms was proposed, considering them as colonial organisms, i.e., each worm was believed to represent a linear colony of numerous zoids (individuals). In other words, each proglottis was recognized as an individual. This view is known as the "polyzoic" concept or theory. The majority of recent workers do not support it. However, the terms arising from this concept, "monozoic" (for cestodes with a single set of genital organs per body) and "polyzoic" (for cestodes with proglottides), are widely used for describing the organization of the body of the tapeworms. Thus, Gyrocotylidea, Amphilinidea, and Caryophyllidea are monozoic, and the remaining orders (excluding Spathebothriidea exhibiting intermediate features) are polyzoic.

Tapeworms lack a gut during all the stages of their development. They feed through the tegument covering the body. Under the tegument, there are several layers of superficial musculature (usually three). Inside, most of the body is made up of parenchyma. Powerful longitudinal muscular bundles, responsible for the movements of the body, pass along the entire strobila. They separate the parenchyma in the center of each proglottis from that in the periphery (the relevant parts of the parenchyma are named medullar and cortical). The nervous system is represented by paired ganglia situated in the scolex and arising from them major anterior and posterior longitudinal nerves, the latter running through the strobila. There are also numerous transverse commissures connecting longitudinal nerves and smaller nerves emanating from them and reaching to the musculature and the receptors.

The excretory system includes flame cells scattered in the parenchyma. Small ducts connect these cells with the major longitudinal canals of the system passing along the strobila. Usually, the longitudinal canals are two dorso-lateral and two ventro-lateral. In addition to the excretion of metabolic products, this system also eliminates the excess water from the body of the worm. By this reason, it also is known as osmoregulatory system.

As a rule, each mature proglottis (or each body of a monozoic cestode) contains one male reproductive system and one female reproductive system.

The male reproductive system includes testes, from one in the genus Aploparaksis (Hymenolepididae) to several hundreds in the genus Taenia (Taeniidae). Each testis is provided with a narrow outgoing duct (vas efferens). These ducts unite into a common wider duct (vas deferens), which transports the sperm to the male copulatory organ. The vas deferens leads into a muscular pouch (cirrus pouch) containing the copulatory organ (cirrus). Along its course, vas deferens may form seminal vesicles before entering the cirrus pouch (external seminal vesicle) and (or) within it (internal seminal vesicle), or to be highly convoluted, in order to have greater sperm storage capacity. The cirrus is a muscular organ, often with spines on its surface. It is able to invaginate (to be withdrawn) in the cirrus pouch or to evaginate (project) through the pore of the cirrus sac.

The female reproductive system consists of ovary, vitellarium, ootype, uterus, vagina, seminal receptacle, and ducts connecting them. The sperm enters the female reproductive system through the vagina during the copulation and is stored in the seminal receptacle. The ovary is variable in location, shape, and size. As oocytes mature, they pass from the ovary into the oviduct. A narrow duct coming from the seminal receptacle joins to the oviduct, which is the place of the fertilization. Vitellarium may be a compact organ (in Cyclophyllidea, Tetrabothriidea, and Nippotaeniidea) or may consist of numerous vitelline follicles scattered in the parenchyma and possessing outgoing ducts uniting into a common vitelline duct (in the majority of orders). The vitelline duct also is connected with the oviduct, and one or more vitelline cells join to each zygote. Together they pass into the ootype. It is usually surrounded by glandular tissue (known as Mehlis's gland) producing a secretion, forming a thin envelope encompassing the zygote and associated vitelline cells. The young eggs pass from the ootype through the uterine duct into the uterus where they complete their development. In the majority of the tapeworms, the eggs leave the final host together with the proglottis in which they have developed. However, some cestodes have uterine pores and eggs can be released one by one.

Distribution

The tapeworms are widespread throughout the world. They occur in almost all terrestrial, marine, brackish, and freshwater habitats where vertebrate animals live. Their diversity appears to be great but poorly explored at the tropical latitudes (most of the newly described species during the last decade originate from tropical habitats). They also are abundant at the temperate latitudes (e.g., the number of species found in terrestrial and freshwater habitats in Europe exceeds 900, and the number of the species recorded from a small territory such as Bulgaria (southeastern Europe) is 310).

More than hundred species were reported from marine birds and mammals in Arctic and Antarctic habitats.

About one third of the cestode species are parasites of marine fishes, mostly of sharks and rays. Several pseudophyllideans were described from deep-sea teleost fishes (e.g., Probothriocephalus alaini was collected at a depth of 2,590–3,350 ft (790–1,020 m), Probothriocephalus muelleri and Phylobythoides stunkardi at a depth between 5,550 and 7,520 ft (1,690 and 2,290 m), all from the North Atlantic).

The cestode orders have cosmopolitan distributions, with three exceptions only. The litobothriideans are known from the Pacific Ocean only, off California, Mexico, and Australia. The nippotaeniideans were recorded from freshwater fishes in Japan, China, Russian Far East, and New Zealand. The haplobothriideans have the most restricted geographical range. The two species of this order occur in North America, in the "living fossil" bowfin (Amia calva).

Habitat

When considering habitats of parasitic organisms, parasitologists make difference between microhabitats and macrohabitats. The microhabitat of a parasite species is an organ or a tissue in the host inhabited by parasite individuals. In broader sense, the whole host individual also could be recognized as a microhabitat. The macrohabitat of a parasite species is that place or environment where its hosts (final, intermediate, and paratenic) live.

The usual microhabitat of the adult tapeworms is the intestine of vertebrate animals. Only the species of the order Amphilinidea inhabit the body cavity of their final hosts (fishes and turtles). Some species of the order Cyclophyllidea occur in other parts of the digestive system (e.g., Cloacotaenia megalops [Hymenolepididae] lives in the cloaca of ducks, Thysanosoma actinioides [Thysanosomatidae] inhabits the bile ducts of ruminants, and Gastrotaenia cygni [Hymenolepididae] occurs under the horny lining of the gizzard of swans).

The intestine of vertebrate animals is not a homogeneous habitat. Its portions differ from each other by their content of nutrients, range of enzymes, pH, and structure of the intestinal wall. It is known for many cestode species that they can be found only in a certain portion of the intestine, e.g., in the duodenum or in the most posterior part (at the ileocaecal junction). A detailed study on the distribution of the parasitic worms along the small intestine of grebes in Canada showed that each of four grebe species was parasitized by 9–17 tapeworm species. Some of these occurred in a high proportion of the intestine that could be interpreted as a broad tolerance for conditions along it. A quarter of cestode species, however, occupied portions no longer than 20% of the intestine length.

Tapeworm larvae have diverse locations in intermediate hosts. Species occurring in crustaceans or insects are usually in the body cavity. The members of the family Taeniidae are parasitic in carnivore mammals and humans and their larvae develop also in mammals. Depending on the cestode species, the larvae of taeniids can be situated in the liver, lungs, musculature, body cavity, brain, and mesentery, sometimes even in the eyes. The most typical locations of cestode larvae in fishes are the musculature, body cavity, and gall bladder.

Concerning the range of the final hosts of cestodes, it is not exaggerated to say that they are not recorded only in vertebrate species, which have not been examined. Only the Cyclostomata (lampreys and hagfishes) have no cestode parasites.

Each tapeworm species is characterized by its host spectrum. This phenomenon is usually marked as "parasite specificity to the host," or simply as "host specificity." Some cestode species are found in one vertebrate species only (oioxenous parasite species). A good example is Dollfusilepis hoploporus (Hymenolepididae). This worm lives in the great crested grebe (Podiceps cristatus) only, even in lakes where this host co-occurs with other grebe species. Other cestode species are found in a small group of related host species belonging to one genus or one family (stenoxenous parasite species) (e.g., Tatria biremis [Amabiliidae] occurs in Eurasia and America in three species of grebes). The majority of tapeworm species are stenoxenous. A few cestodes are euryxenous parasites, i.e., live in unrelated (phylogenetically distant) hosts. In the latter case, a prerequisite for the formation of such parasite-hosts associations is the convergence of the ecology (in terms of similar habitats and diets) of the hosts. An example for this can be Ligula intestinalis (Diphyllobothriidae) occurring as adult in birds of various orders: gulls of Charadriiformes, herons of Ciconiiformes, grebes of Podicipediformes, cormorants of Pelecaniformes, and mergansers of Anseriformes. However, the infective larvae of this parasite live in fishes of the family Cyprinidae only. Therefore, L. intestinalis is euryxenous relative to the final hosts but stenoxenous relative to the second intermediate host.

A few tapeworm species are known that mature in invertebrate animals. Thus, Archigetes sieboldi, Archigetes limnodrili, and Archigetes iowensis (Caryophyllidea) can mature in the body cavity of freshwater annelids, and Diplocotyle olriki and Cyathocephalus truncatus (Spathebothriidea) in amphipod crustaceans. The same invertebrate groups are intermediate hosts of the two cestode orders. Alternatively, all these forms can mature in the intestine of fishes (final hosts). The life cycles with the participation of only one invertebrate host are considered secondarily simplified, allowing shortening time needed for maturation of worms in the final host. However, there are data showing that at least some of these species can live in water basins where appropriate fish final hosts are lacking.

Macrohabitats of tapeworms are diverse, from deep sea to high mountains and from tropical forests to tundra. There are even species living in extreme conditions (e.g., several species parasitizing flamingos, avocets, and plovers live as larvae in brine shrimps [Artemia spp.] in salinas. Such species is Flamingolepis liguloides [Hymenolepididae]).

Behavior

Little is known about the behavior of tapeworms in the intestine of the host. It seems that most of the tapeworms are permanently attached during their entire life at a certain site of the intestinal wall. However, there are well-documented observations on circadian migrations of Hymenolepis diminuta (Hymenolepididae) from one microhabitat to another in the intestine of rats. This migration depends on the host feeding and digestion. When the gut of the rat is empty, the worms of this species are situated in the posterior region of the small intestine. However, as the content of the stomach passes into the intestine, they rapidly migrate towards the duodenum.

Feeding ecology and diet

All the cestodes feed through the body surface. The nutrient molecules (carbohydrates as glucose and galactose, amino acids, purines and pyrimidines, fatty acids, monoglycerides, sterols, and some vitamins) are absorbed through the tegument.

Reproductive biology

The majority of cestodes are hermaphroditic (only the members of the tetraphyllidean family Dioecotaeniidae and the cyclophyllidean family Dioecocestidae are dioecious). As a rule, each proglottis contains one set of male reproductive organs and one set of female reproductive organs. Often the maturation of the male organs and female organs do not coincide in time. In the majority of the families, the male organs mature first and proglottides initially act as male. This type of strobilar development is known as protandry. In some families (e.g., in the Progynotaeniidae), female reproductive organs develop first. In the latter case, the sperm production in testes coincides with the development of the eggs in the uterus. This type of development is known as proterogyny. Both types of strobilar development should be considered adaptations allowing more complete utilization of resources—though hermaphroditic, each proglottis is initially functionally male and after that functionally female (or visa versa), thus being able to produce larger number of gametes. It also prevents self-fertilization.

The life cycle of each cestode species includes at least two hosts, final and intermediate. The final or definitive host is that harboring adult (reproducing sexually) worms. The intermediate host is that where larvae (known also as metacestodes) develop. The two hosts are in close ecological associations, facilitating the transmission of the parasite. The intermediate host lives in habitats where the final host feeds and defecates. The intermediate host is also a common component of the diet of the final host. The transmission of the cestode from the intermediate host to the final host is along the food chains only. Often the transmission is facilitated by a parasite-induced modification of the intermediate host's behavior, color, or health condition, in order to make it easier prey for the final host.

The general scheme of the life cycle is as follows. The cestode eggs pass with host's feces into the environment. Each egg encompasses an embryo named oncosphere. The latter possesses six embryonic hooks and several glandular cells and is surrounded by several envelopes. The egg is eaten by the intermediate host. In the gut of this host, the oncosphere hatches and, using its hooks and glands, penetrates through the intestinal wall and locates in the body cavity or in any internal organ. There, it metamorphoses into an infective larval stage (metacestode). In the most common case, the metacestode has a fully developed scolex identical to that of the adult worm. The final host is infested by eating infected intermediate hosts. The scolex of the metacestode attaches to the intestinal wall of the final host. The neck of the worms starts the production of proglottides and thus the strobila is formed. With the further development of the proglottides, the worm starts producing eggs, which are released with feces into the environment.

There are numerous cestode species exhibiting details in the life cycle differing from that described in the general scheme. Some species have two intermediate hosts or mobile embryos able to swim (see the account for Diphyllobothrium latum). The embryos of Amphilinidea and Gyrocotylidea are not oncospheres but lycophoras (see the account for Amphilina foliacea). The range of the intermediate hosts used is also impressive.

Metacestodes of various orders and families exhibit an immense morphological variability. Procercoid is the metacestode in the first intermediate host that has an elongate body and cercomer (e.g., in Pseudophyllidea). Entering into the second intermediate host, it develops into the plerocercoid. The latter possesses a differentiated scolex and is able to infect the final host. Embryos of other cestodes directly develop into plerocercoids (e.g., Proteocephalidea and Nippotaeniidea).

The most widespread type of metacestodes in the order Cyclophyllidea is the cysticercoid. It is a solid-bodied organism with fully developed scolex retracted into the body. Among the Taeniidae, the most widespread metacestode is the cysticercus. Its scolex is introverted.

As in 2001, life cycles of about 200 cestode species are known (out of 5,100–5,200 species described). Obviously, the discovery of their enormous diversity, in terms of the range of hosts utilized and the morphological specialization of metacestodes, is a matter for the future.

Conservation status

No cestode species is listed by the IUCN.

Significance to humans

A total of 57 cestode species were reported from humans. Some of these are not "true" parasites of humans (the infections with them are accidental). However, six species are considered of great public health significance because they are agents of serious and widespread diseases. In 1999, when the human population was almost 6 billion persons, the estimate of the numbers of infected humans (in millions) was as follows: Taenia saginata—77.0, Hymenolepis nana—75.0, Taenia solium —10.0, Diphyllobothrium latum—9.0, and Echinococcus granulosus and Echinococcus multilocularis (considered together)—2.7.

Numerous cestode species are of primary importance for veterinary medicine. Several species of Taeniidae are major parasites of domestic ruminants (Echinococcus granulosus, Taenia multiceps, T. hydatigena, and T. ovis). Members of the family Anoplocephalidae are important parasites of horses, ruminants, and rabbits. Some taeniids, mesocestoidids, and dipylidiids are frequent parasites of dogs and cats. Among the parasites of domestic birds, the most common are members of the families Hymenolepididae and Davaineidae.

Cestodes of the order Caryophyllidea, Pseudophyllidea, and Proteocephalidea may cause significantly reduced production in fish farming operations.

Species accounts

List of Species

No common name

Amphilina foliacea

order

Amphilinidea

family

Amphilinidae

taxonomy

Monostomum foliaceum Rudolphi, 1819, Italy.

other common names

None known.

physical characteristics

Body monozoic, dorso-ventrally flattened, oval or leaf-shaped in outline, 1–2.6 in (28–65 mm) long and 0.67–1.2 in (17–30 mm) wide. Anterior end pointed, with slightly expressed apical invagination. Uterine orifice situated in anterior end. Orifice of ejaculatory duct on posterior end. Vaginal pore postero-lateral, at some distance from male pore.

distribution

Europe and Siberia.

habitat

Adults are parasitic in the body cavity of sturgeons (Acipenser sturio, A. nudiventris, A. ruthenus, A. stellatus, Huso huso, etc.). Larvae develop in freshwater amphipod crustaceans. The macrohabitats of Amphilina foliacea are large rivers in Eurasia. Though it cannot develop in marine amphipods, it can be found also in marine sturgeons (which are anadromous).

feeding ecology and diet

Not studied. Apparently absorb nutrients through the tegument.

behavior

Nothing is known.

reproductive biology

A. foliacea is hermaphroditic. There are no data how often cross-fertilization or self-fertilization may occur. Eggs develop in uterus and are released through its orifice. Each egg contains larva named lycophora. It is not known how eggs pass from the body cavity of the sturgeon into the water. The eggs are swallowed by amphipods (intermediate hosts). The lycophora leaves the egg envelope in the intestine of the intermediate host and passes through its wall into the body cavity. There, it develops into a larva (about 0.16 in [4 mm] long) for some six weeks. Feeding on crustaceans containing fully developed larvae infects sturgeons. Larvae pass through the wall of the stomach into the body cavity. They become mature after six to seven months and live several years.

conservation status

Not listed by the IUCN.

significance to humans

None known.

No common name

Caryophyllaeus laticeps

order

Caryophyllidea

family

Caryphyllaeidae

taxonomy

Taenia laticeps Pallas, 1781, Russia.

other common names

None known.

physical characteristics

Body monozoic, longitudinally elongate, 0.79–1.6 in (20–40 mm) long and 0.04–0.08 in (1–2 mm) wide. Anterior end wider, forming some folds. Male genital pore and female genital pore situated on the ventral surface of the body at some distance from its posterior end.

distribution

North Eurasia, in Europe, Siberia, Central Asia, and Russian Far East.

habitat

Originally described as a parasite of the common bream (Abramis brama). Known also from about 30 species of freshwater fishes, mostly of the family Cyprinidae. Recorded also in some predatory fishes belonging to other families (e.g., pike and perch). Larvae recorded in tubificid annelids. The macrohabitats are slow rivers, lakes, ponds, marches, reservoirs, etc.

feeding ecology and diet

Internal parasite absorbing nutrients through the tegument.

behavior

Nothing is known.

reproductive biology

Caryophyllaeus laticeps is hermaphroditic. Eggs released with feces of the final hosts (fishes) need to stay in water for about three months in order to become infective. Intermediate hosts (aquatic tubificids) become infected by eating them. The oncosphere hatches in the intestine and penetrates into the body cavity. The larva develops for about six months. When fully developed, it is about 0.08 in (2 mm) long, with primordia of reproductive organs. Eating tubificids containing larvae infects fishes.

conservation status

Not listed by the IUCN.

significance to humans

Together with another parasite of the same genus (C. fimbriceps), C. laticeps may cause a disease of farmed carps known as caryophyllaeasis. If parasites are few, they are not pathogenic for the host. It is believed that about 20 parasites per fish may cause some disorders of the digestive system and anemia.

No common name

Tatria biremis

order

Cyclophyllidea

family

Amabiliidae

taxonomy

Tatria biremis Kowalewski, 1904, Ukraine.

other common names

None known.

physical characteristics

Body 0.08–0.16 in (2–4 mm) long and 0.02–0.03 in (0.6–0.8 mm) wide. Strobila consists of 20–30 proglottides. Rostellum, bearing 10 hooks, can protrude very much in order to penetrate deeply into the intestine wall.

distribution

Eurasia and North America.

habitat

Parasite of grebes, mostly of Podiceps auritus, P. nigricollis, and P. grisegena. Larvae recorded in aquatic insects. The macrohabitats include freshwater lakes and slow rivers.

feeding ecology and diet

Internal parasite absorbing nutrients through the tegument.

behavior

Nothing is known.

reproductive biology

Tatria biremis is hermaphroditic. Gravid proglottides are released into the environment with feces. They are eaten by aquatic insects which are intermediate hosts of this parasite. The only record of larvae is from Sigara concinna (Heteroptera, Corixidae) from Kazakhstan.

conservation status

Not listed by the IUCN.

significance to humans

None known

No common name

Moniezia benedeni

order

Cyclophyllidea

family

Anoplocephalidae

taxonomy

Taenia benedeni Moniez, 1879, France.

other common names

None known.

physical characteristics

Body 8.2–13 ft (2.5–4 m) long and 0.99–1.0 in (25–26 mm) wide. Scolex with four suckers, without rostellum. Proglottides

transversely elongate. Each proglottid has two sets of reproductive organs, including two genital pores situated on both lateral margins.

distribution

Cosmopolitan.

habitat

Microhabitats of adult worms are intestines of domestic (cattle, sheep, goats) and some wild ruminants (moose, antelopes, deer, etc.). Larvae develop in oribatid mites. Macrohabitats include grasslands, forests, and pastures.

feeding ecology and diet

Internal parasite absorbing nutrients through the tegument.

behavior

Nothing is known.

reproductive biology

This species is hermaphroditic. Oribatid mites are infected by eating eggs of the parasite. Depending on the temperature, larvae (cysticercoids) develop in them for four to seven months. Ruminants eat infected mites while grazing on grass. Worms become mature after about 50 days.

conservation status

Not listed by the IUCN.

significance to humans

This and another parasite of the same genus, M. expansa, are agents of a disease (monieziasis) of sheep, goats, and cattle. It is more dangerous for young animals than for adults. Histological changes of the intestinal walls and intoxication of the infected animals have been described.

No common name

Davainea proglottina

order

Cyclophyllidea

family

Davaineidae

taxonomy

Taenia proglottina Davaine, 1860, France.

other common names

None known.

physical characteristics

Body 0.02–0.04 in (0.5–1.0 mm) (sometimes up to 0.12 in [3 mm]) long. Scolex with four suckers armed with spines and rostellum armed with 60–90 hammer-shaped rostellar hooks. Proglottides, five to nine, usually six in number.

distribution

Cosmopolitan.

habitat

Adults in intestines of poultry. Larvae in the body cavity of slugs. This parasite is very common in farms in humid areas where slugs are abundant.

feeding ecology and diet

Internal parasite absorbing nutrients through the tegument.

behavior

Nothing is known.

reproductive biology

Each adult parasite produces one gravid proglottis per day, which is released with feces of the final host. Slugs, which are often coprophagous, eat gravid proglottides. The development of the larva (named cysticercoid) continues in the body cavity of the mollusk for 15–22 days (depending on temperature regime). Hens are infested as a result of eating infected slugs. Worms mature in the intestine of the final host for 12–16 days.

conservation status

Not listed by the IUCN.

significance to humans

Davainea proglottina causes a parasitic disease of poultry. Its pathogenesis is mostly connected with an inflammation of the duodenum. Its acute phase continues three to five days. The mortality can reach up to 60%.

No common name

Progynotaenia odhneri

order

Cyclophyllidea

family

Progynotaeniidae

taxonomy

Progynotaenia odhneri Nybelin, 1914, Sweden.

other common names

None known.

physical characteristics

Body minute, 0.08–0.12 in (2–3 mm) long and 0.02–0.03 in (0.6–0.8 mm) wide, wedge-shaped. Strobila consisting of 8–12 proglottides. Scolex provided with rostellum bearing 12 rostellar hooks. Genital pores on the lateral margins of the proglottides, regularly alternating on the left and the right sides.

distribution

Eurasia and Africa.

habitat

Parasitic in plovers, mostly in ringed plover (Charadrius hiaticula) and snowy plover (Charadrius alexandrinus). Most of the records are from seashores or salt lakes, which seem to be the macrohabitats of this parasite.

feeding ecology and diet

Intestinal parasite absorbing nutrients through the tegument.

behavior

Nothing is known.

reproductive biology

Progynotaenia odhneri is hermaphroditic. However, it does not possess a vagina. The copulation is traumatic: the heavily armed cirrus penetrates through the tegument and the parenchyma and directly inseminates the seminal receptacle. The intermediate hosts of this species are not known.

conservation status

Not listed by the IUCN.

significance to humans

None.

Dog tapeworm

Echinococcus granulosus

order

Cyclophyllidea

family

Taeniidae

taxonomy

Hydatigena granulosa Batsch, 1786, Germany.

other common names

French: Ténia échinocoque; German: Hülsenwurm.

physical characteristics

Adult 0.12–0.24 in (3–6 mm) long, consisting of scolex, short neck, and three to five proglottides. Scolex bearing 30–36 (rarely more) rostellar hooks. Gravid proglottis highly elongate.

distribution

Cosmopolitan.

habitat

Microhabitats are intestines of carnivore mammals, mostly of the family Canidae (dogs, wolves, jackals, etc). Larvae occur in internal organs (liver, lungs, musculature) of herbivorous mammals. Macrohabitats include natural ecosystems where parasites circulate along the food chain wild herbivores—wild carnivores or in habitats associated with humans (pastures, farms, villages) where major final hosts are dogs and intermediate hosts are domestic animals (sheep, cattle, camels, pigs, goats, horses, etc.).

feeding ecology and diet

Internal parasite absorbing nutrients through the tegument.

behavior

The released gravid proglottis is able to crawl. Some data indicate that such proglottides may climb up grasses, where they are able to disperse their eggs more efficiently and contaminate a larger area of grassland. Some gravid proglottides may stay around the anus of the dog, contaminating its fur with eggs.

reproductive biology

Oncospheres hatching from eggs in the intestine of the intermediate host migrate to the liver or the lungs, sometimes to the musculature or even to the eyes. They grow very slowly and transform into a cyst named "unilocullar hydatid." Its wall consists of two layers. The inner layer is able to produce numerous scoleces (i.e., asexual reproduction occurs during the larval development). The inner layer also is able to produce daughter cysts, situated within the mother cyst, which also can produce numerous scoleces. The development of the hydatid may continue for 20–30 years. When a carnivorous mammal eats a liver or another organ containing a hydatid, it becomes infected. In its intestine, each scolex produces an adult tapeworm.

conservation status

Not listed by the IUCN.

significance to humans

Echinococcosis, or hydatid disease, is one of the most serious parasitic diseases of human in Asia, Africa, South America, and Europe. Humans are infected as intermediate hosts, i.e., hydatids develop in the internal organs. Some recent attempts for drug treatment are very promising. However, in 2000–2002, surgery remains the only routine method of treatment.

Echinococcus granulosus is also of primary veterinary importance because the hydatid disease is dangerous for many domestic herbivores (sheep, pigs, goats, cattle, camels, horses, etc.).

Beef tapeworm

Taenia saginata

order

Cyclophyllidea

family

Taeniidae

taxonomy

Taenia cucurbitina grandis saginata Goeze, 1782, Germany. Taeniarhynchus saginatus (Goeze, 1782) Weinland, 1858.

other common names

French: Ténia inerme; German: Rinderbandwurm.

physical characteristics

Body usually 9.8–16 ft (3–5 m) long (exceptionally, some specimens reach a length of 66 ft [20 m]), with maximum width (0.20–0.28 in [5–7 mm]) at gravid proglottides. Scolex lacks rostellum and hooks. Gravid proglottides (found in feces of humans) can be distinguished from those of the other common human Taenia, T. solium, by the uterus having 15–20 (or more) lateral branches (versus 7–13 lateral branches in T. solium).

distribution

Cosmopolitan.

habitat

The microhabitats of this species are the intestines of humans (for adult worms) and the body musculature of cattle (for larvae). The macrohabitats can be all places where uninspected raw or undercooked beef is eaten, or where cattle graze on grass contaminated by eggs released with human feces.

feeding ecology and diet

Internal parasite absorbing nutrients through the tegument.

behavior

The gravid proglottis can migrate out of the anus of the infected human and then can be found in the bed or in the underpants. However, it is usually released with feces. It actively crawls and can go at some distance from feces. With drying up, a rupture appears on the ventral surface of the proglottis, allowing eggs to disperse in the environment.

reproductive biology

Russian researchers carried out a long-term study on the egg production of T. saginata in infected humans, including by provoking experimental self-infections during the period 1930–1940. They found that the adult parasite could live in the human intestine for more than 10 years. The daily output can reach up to 28 proglottides. Each proglottis may contain up to 175,000 eggs. Thus, an infected person may release up to 5 million eggs per day. Eggs are eaten by cattle with contaminated grass. They hatch in the duodenum. Oncospheres penetrate through the intestinal wall and enter blood vessels. They reach the musculature and turn into infective larvae (cysticerci) in about 8–10 weeks. Humans become infected by eating beef containing alive cysticerci (raw or undercooked). The adult worms start to produce gravid proglottids about one to three months after entering the final host.

conservation status

Not listed by the IUCN.

significance to humans

Among tapeworms, T. saginata is the most widespread agent of parasitic diseases of humans in the world. The parasitic disease caused by it is known as taeniiasis or taeniarhynchiasis. The latter originates from the name of the genus Taeniarhynchus where this parasite was placed before 1994. The validity of this genus is not supported by most authors publishing since then.

Most of the infected people have no symptoms (except releasing gravid proglottides). Sometimes symptoms such as abdominal pain, diarrhea, headache, loss of appetite, and allergic reactions may occur. Several anthelmintic drugs are very efficient against this worm. The prevention is not difficult: beef is not dangerous when fully cooked and no longer pink inside. Cysticerci are killed at 131–140°F (55–60°C).

An alternative viewpoint of the significance of T. saginata (and the other two species using humans as final hosts, T. solium and T. asiatica, both with larvae developing in pigs) to humankind may be relevant. The traditional opinion among scientists is that with the domestication of intermediate hosts (cattle and swine) the species of Taenia have become associated with humans (some 10,000 years ago). However, phylogenetic studies during 2000–2001 based on comparative morphology and gene sequences suggest that hominids obtained taeniids before the origin of the modern humans. Probably some 2 million years ago, large African hominids preyed on antelopes and other bovids in the savanna, where large cats and hyenas also lived. They were parasitized by taeniid tapeworms because of their similar diet with that of the carnivore mammals. Once hominids acquired taeniid tapeworms, they also contributed to the rate of the infestation of herbivore mammals by providing additional tapeworm eggs in the grasslands. Wild bovids, with their musculature heavily infected by cysticerci, were probably easier prey than uninfected animals. Thus, T. saginata (or its ancestor living in our ancestors) helped early hominids have meat on their menu more frequently. At least part of the evolutionary success of our species may be due to tapeworms!

No common name

Proteocephalus longicollis

order

Proteocephalidea

family

Proteocephalidae

taxonomy

Alyselmintus longicollis Zeder, 1800, type locality unknown.

other common names

None known.

physical characteristics

Body up to 8.7 in (220 mm) long and about 0.06–0.08 in (1.5–2 mm) wide. Scolex small (diameter up to 0.016 in [0.4 mm]), provided with small suckers and small sucker-like apical organ. Gravid proglottides up to 0.06–0.08 in (1.5–2 mm) long. Genital pores on the lateral margins of proglottides, irregularly alternating.

distribution

Eurasia and North America.

habitat

The microhabitats are the intestines of freshwater fishes (Salmonidae, Coregonidae, and Osmeridae, sometimes in others). This species inhabits lakes and rivers in the Northern Hemisphere.

feeding ecology and diet

Internal parasite absorbing nutrients through the tegument.

behavior

Nothing is known.

reproductive biology

This species is hermaphroditic. Eggs released in water are eaten by copepods, which are intermediate hosts. The infective larva develops in the body cavity of the crustacean. The fishes become infected by eating copepods containing cestode larvae.

conservation status

Not listed by the IUCN.

significance to humans

Parasitic in fishes, including in those in fish farms. No data of economic significance.

Broad fish tapeworm

Diphyllobothrium latum

order

Pseudophyllidea

family

Diphyllobothriidae

taxonomy

Taenia lata Linnaeus, 1758, type locality unknown.

other common names

German: Fischbandwurm.

physical characteristics

Polyzoic. Strobila with length about 30 ft (9 m) (there are data about specimens reaching up to 66 ft [20 m]), consisting of 3,000–4,000 proglottides. Scolex finger-shaped, with two bothria. Uterus rosette-shaped in gravid proglottides.

distribution

Scandinavia, Baltic States, Russia, United States and Canada (Great Lakes area, Pacific Coast, Arctic), Ireland, Japan, around some lakes and large rivers in Africa, and South America.

habitat

Adults are common intestinal parasites of fish-eating mammals (dogs, cats, bears, seals, humans). Larvae develop in crustaceans (first intermediate hosts) and fishes (second intermediate hosts). The macrohabitats include rivers and freshwater lakes.

feeding ecology and diet

Internal parasite absorbing nutrients through the tegument.

behavior

Nothing is known.

reproductive biology

As almost all cestodes, this species is hermaphroditic. Eggs are released through the uterine pore and pass into the environment with feces of the host. The embryo encompassed in the egg needs one or several weeks (depending on the temperature) to become infective. The fully developed embryo (known as coracidium) hatches from the egg in water. It is covered by ciliated epidermis and can swim several hours until being eaten by a copepod crustacean (first intermediate host). In the intestine of the copepod, the coracidium loses its ciliated cover and penetrates into the body cavity. There, the embryo feeds on the nutrients contained in the hemolymph. For about 20–25 days, it turns into an elongate larva (procercoid, up to 0.0197 in [500 µm] long) possessing a cercomer at its posterior end. The procercoid is pathogenic for the copepod in terms of interfering with its motility and thus turning it into an easy prey for fishes. When the infected copepod is eaten by a fish (second intermediate host), the procercoid migrates from the intestine into the body musculature and turns into the next larval stage (plerocercoid). The predation of infected fishes, or even eating undercooked fish dishes in a restaurant, is the way of the transmission of the plerocercoid (from several millimeters to a few centimeters long) to the final host. In the host's intestine, the worm grows and becomes mature for some two weeks.

conservation status

Not listed by the IUCN.

significance to humans

This species is of great medical importance. The disease caused by it is named diphyllobothriasis. Among the most widespread parasitic diseases caused by tapeworms, it is ranked fourth. Its symptoms are diarrhea, abdominal discomfort, and weakness, in some cases anemia. The contemporary drug treatment is very efficient.

No common name

Phyllobothrium squali

order

Tetraphyllidea

family

Phyllobothriidae

taxonomy

Phyllobothrium squali Yamaguti, 1952, off Onahama, Japan.

other common names

None known.

physical characteristics

Body 5.5–24 in (14–60 cm) long, 0.08–0.16 in (2–4 mm) wide. Scolex 0.12–0.18 in (3–4.5 mm) wide, with four foliose bothridia with folded margins. Anterior end of each bothridium provided with small sucker. Apex of the scolex provided with glandular organ. Genital pores on lateral margins of proglottides, irregularly alternating.

distribution

Japanese waters, Black Sea, and Irish Sea.

habitat

In the spiral intestine of piked dogfish, Squalus acanthias (Squaliformes, Squalidae).

feeding ecology and diet

Internal parasite absorbing nutrients through the tegument.

behavior

Nothing is known.

reproductive biology

Hermaphroditic. The life cycle is unknown.

conservation status

Not listed by the IUCN.

significance to humans

None known.

Resources

Books

Brooks, D. R., and D. A. McLennan. Parascript: Parasites and the Language of Evolution. Washington and London: Smithsonian Institution Press, 1993.

Combes, C. Parasitism: The Ecology and Evolution of Intimate Interactions. Chicago and London: University of Chicago Press, 2001.

Gibson, D. I., R. A. Bray, and C. B. Powell. "Aspects of the Life History and Origins of Nesolecithus africanus (Cestoda: Amphilinidea)." Journal of Natural History 21 (1987): 785–794.

Hoberg, E. P., N. L. Alkire, A. de Queiroz, and A. Jones. "Out of Africa: Origins of the Taenia Tapeworms in Humans." Proceeding of the Royal Society, London. Series B 268 (2000): 781–787.

Kearn, G. C. Parasitism and the Platyhelminths. London: Chapman and Hall, 1998.

Khalil, L. F., A. Jones, and R. A. Bray. Keys to the Cestode Parasites of Vertebrates. Wallingford: CAB International, 1994.

Littlewood, D. T. J., and R. A. Bray, eds. Interrelations of the Platyhelminthes. London and New York: Taylor and Francis, 2001.

Roberts, L. S., and J. Janovy. Gerald D. Schmidt and Larry S. Roberts' Foundations of Parasitology. 6th ed. Boston: McGraw-Hill Co., 2000.

Ruppert, E. E., and R. D. Barnes. Invertebrate Zoology. 6th ed. Forth Worth, TX: Saunders College Publishing, 1994.

Schmidt, G. D. CRC Handbook of Tapeworm Identification. Boca Raton, FL: CRC Press, Inc., 1986.

Scholz, T., and V. Hanzelová. Tapeworms of the Genus Proteocephalus Weinland, 1858 (Cestoda: Proteocephalidae), Parasites of Fishes in Europe. Prague: Academia, 1998.

Periodicals

Bandoni, S. M., and D. R. Brooks. "Revision and Phylogenetic Analysis of the Amphilinidea Poche, 1922 (Platyhelminthes: Cercomeria: Cercomeromorpha)." Canadian Journal of Zoology 65 (1987): 1110–1128.

Beveridge, I., and R. A. Campbell. "Redescription of Diesingium lomentaceum (Diesing, 1850) (Cestoda: Trypanorhyncha)." Systematic Parasitology 27 (1994): 149–157.

Caira, J. N., K. Jensen, and C. J. Healy. "On the Phylogenetic Relationships Among Tetraphyllidean, Lecanicephalidean and Diphyllidean Tapeworm Genera." Systematic Parasitology 42, no. 2 (February 1999): 77–151.

Cañeda–Guzmán, I. C., A. Chambrier, and T. Scholz. "Thaumasioscolex didelphidis n.gen., n.sp. (Eucestoda: Proteocephalidae) from the Black-eared Opossum Didelphis marsupialis from Mexico, the First Proteocephalidean Tapeworm from a Mammal." Journal of Parasitology 87, no. 3 (June 2001): 639–646.

Crompton, D. W. T. "How Much Human Helminthiasis Is There in the World?" Journal of Parasitology 85, no. 3 (June 1999): 397–403.

Faliex, E., G. Tyler, and L. Euzet. "A New Species of Ditrachybothridium (Cestoda: Diphyllidea) from Galeus sp. (Selachii, Scyliorhynidae) from the South Pacific Ocean, with a Revision of the Diagnosis of the Order, Family, and Genus and Notes on Descriptive Terminology of Microtriches." Journal of Parasitology 86, no. 5 (October 2000): 1078–1084.

Hanzelová, V., and T. Scholz. "Species of Proteocephalus Weinland, 1858 (Cestoda: Proteocephalidae), Parasites of Coregonid and Salmonid Fishes from North America: Taxonomic Reappraisal." Journal of Parasitology 85, no. 1 (February 1999): 94–101.

Hoberg, E. P. "Phylogenetic Relationships Among Genera of the Tetrabothriidae (Eucestoda)." Journal of Parasitology 75, no. 4 (August 1989): 617–626.

Hoberg, E. P., S. L. Gardner, and R. A. Campbell. "Systematics of the Eucestoda: Advances Toward a New Phylogenetic Paradigm, and Observations on the Early Diversification of Tapeworms and Vertebrates." Systematic Parasitology 42, no. 1 (January 1999): 1–12

Hoberg, E. P., J. Mariaux, J.-L. Justine, D. R. Brooks, and P. J. Weekes. "Phylogeny of the Orders of the Eucestoda (Cercomeromorphae) Based on Comparative Morphology: Historical Perspectives and a New Working Hypothesis." Journal of Parasitology 83, no. 6 (December 1997): 1128–1147.

Jensen, K. "Four New Genera and Five New Species of Lecanicephalideans (Cestoda: Lecanicephalidea) from Elasmobranchs in the Gulf of California, Mexico." Journal of Parasitology 87, no. 4 (August 2001): 845–861.

Justine, J.-L. "Spermatozoa as Phylogenetic Characters for the Eucestoda." Journal of Parasitology 84, no. 2 (April 1998): 385–408.

Littlewood, D. T. J., K. Rohde, and K.A. Clough. "The Interrelations of All Major Groups of Platyhelminthes: Phylogenetic Evidence from Morphology and Molecules." Biological Journal of the Linnean Society 66 (1999): 75–114.

Neifar, L., G. A. Tayler, and L. Euzet. "Two New Species of Macrobothridium (Cestoda: Diphyllidea) from Rhinobatid Elasmobranchs in the Gulf of Gabès, Tunisia, with Notes on the Status of the Genus." Journal of Parasitology 87, no. 3 (June 2001): 673–680.

Nikolov, P. N., and B. B. Georgiev. "The Morphology and New Records of Two Progynotaeniid Cestode Species." Acta Parasitologica 47, no. 2 (June 2002): 121–130.

Olson, P. D., and J. N. Caira. "Two New Species of Litobothrium Dailey, 1969 (Cestoda: Litobothriidea) from Thresher Sharks in the Gulf of California, Mexico, with Redescriptions of Two Species in the Genus." Systematic Parasitology 48, no. 3 (March 2001): 159–177.

Olson, P. D., D. T. J. Littlewood, R. A. Bray, and J. Mariaux. "Interrelations and Evolution of the Tapeworms (Platyhelminthes: Cestoda)." Molecular Phylogenetics and Evolution 19, no. 3 (June 2001): 443–467.

Rego, A. A., A. Chambrier, V. Hanzelová, E. Hoberg, T. Scholz, P. Weekes, and M. Zehnder. "Preliminary Phylogenetic Analysis of Subfamilies of the Proteocephalidea (Eucestoda)." Systematic Parasitology 40, no. 1 (May 1998): 1–19.

Scholz, T., and R. A. Bray. "Probothriocephallus alaini n. sp. (Cestoda: Triaenophoridae) from the Deep-sea Fish Xenodermichthys copei in the North Atlantic Ocean." Systematic Parasitology 50, no. 3 (November 2001): 231–235.

Stock, T. M., and J. Holmes. "Functional Relationships and Microhabitat Distributions of Enteric Helminths of Grebes (Podicipedidae): The Evidence for Interactive Communities." Journal of Parasitology 74, no. 2 (April 1988): 214–227

Tyler, G. A., and J. N. Caira. "Two New Species of Echinobothrium (Cestoidea: Diphyllidea) from Myliobatiform Elasmobranchs in the Gulf of California, Mexico." Journal of Parasitology 85, no. 2 (April 1999): 327–335.

Tyler, G. A. "Diphyllidean Cestodes of the Gulf of California, Mexico with Descriptions of Two New Species of Echinobothrium (Cestoda: Diphyllidea)." Journal of Parasitology 87, no. 1 (February 2001): 173–184.

Vasileva, G. P., G. I. Dimitrov, and B. B. Georgiev. "Phyllobothrium squali Yamaguti, 1952 (Tetraphyllidea, Phyllobothriidae): Redescription and First Record in the Black Sea." Systematic Parasitology 53, no. 1 (September 2002): 49–59.

Vasileva, G. P., D. I. Gibson, and R. A. Bray. "Taxonomic Revision of Tatria Kowalewski, 1904 (Cestoda: Amabiliidae): Redescriptions of T. biremis Kowalewski, 1904 and T. minor Kowalewski, 1904, and the Description of T. gulyaevi n. sp. from Palaearctic Grebes. "Systematic Parasitology 54, no. 3 (March 2003): 177–198.

Organizations

Academy of Sciences of the Czech Republic, Institute of Parasitology. Ceské Budejovice, Czech Republic.<http://www.paru.cas.cz/structure/Lab_of_par_flatworms/index.html>

Agricultural Research Service. Web site: <http://www.ars.usda.gov/is/AR/archive/may01/worms0501.htm>

Bulgarian Academy of Sciences, Central Laboratory of General Ecology. Sofia, Bulgaria. <http://www.diplectanum.dsl.pipex.com/bas/>

Natural History Museum, Department of Invertebrates. Geneva, Switzerland. <http://www.ville-ge.ch/musinfo/mhng/index.htm>

The Natural History Museum, Department of Zoology, Parasitic Worms Division. London, UK. <http://www.nhm.ac.uk/zoology/home/home.htm>

National Museum of Natural History, Laboratory of Biology of Parasites, Protistology and Helminthology. Paris, France. <http://www.mnhn.fr/mnhn/bpph/>

Russian Academy of Sciences, Zoological Institute, Department of Parasitic Worms. St. Petersburg, Russia. <http://www.zin.ru/labs/worms/eng/main_eng2.htm>

U. S. Department of Agriculture, Agricultural Research Service, U. S. National Parasite Collection,.Beltsville, MD USA. <http://www.lpsi.barc.usda.gov/bnpcu/>

University of Connecticut, Department of Ecology and Evolutionary Biology. Storrs, CT USA. <http://collections2.eeb.uconn.edu/tapewormsdotorg/home.htm>

University of Nebraska State Museum, The Harold W. Manter Laboratory of Parasitology. Lincoln, NE USA. <http://www-museum.unl.edu/research/parasitology/>

University of Toronto, Department of Zoology. Toronto, Canada. <http://brooksweb.zoo.utoronto.ca/index.html>

Boyko B. Georgiev, PhD