We will follow the classification scheme utilized by Roberts and Janovy. The classification of platyhelminths is another subject which has changed rapidly in the last decade. When you encounter terms which are unfamiliar refer to your glossary for the definitions.
General Features
Platyhelminthes are the flatworms and get their name from their fact that they are dorsoventrally flattened. Some are oval or leaf-shaped while others, such as the tapeworms, are elongated. They range in length from nearly microscopic to over 50 m. They are acoelomate, but possess mesoderm which gives rise to reproductive organs, musculature and parenchyma of the adults. These worms are bilaterally symmetrical with anterior and posterior ends. There is a fairly well-developed nervous system with associated sensory and motor nerves elements. These worms occupy many niches throughout the world. Many platyhelminth species are free living, but a variety of symbiotic relationships from commensalism to parasitism are common. The inability of flatworms to synthesize fatty acids and sterols may explain their need for establishing symbiotic relationships.
The tegument varies considerably among the groups of flatworms. The free-living turbellaria and free-living stages of parasitic helminths have ciliated epithelia, which is utilized for locomotion for many species. In these flatworms, the epithelium is thin and formed of a single layer of cells with many glandular cells and ducts from subepithelial glands. Duogland adhesive systems are found in some flatworms containing some cells which produce adhesive secretions and other cells which produce releasing secretions. In adult parasitic helminths, the epidermis is a syncytial tegument with the nuclei in cell bodies beneath a superficial muscle layer.
The platyhelminths are acoelomate and most of the body is made up of parenchyma. Parenchyma is a rather loose mass of fibers and cells of several types. Cell functions include secretion, food and waste storage and regeneration. The organs are tightly associated with the parenchyma and are virtually impossible to dissect out. Muscle fibers are found throughout the parenchyma, but are rarely striated. Most fibers are arranged in one or two layers near the body surface, but circular and dorsoventral fibers are also found.
In cestodes and trematodes, the nervous system is arranged like a ladder with paired ganglia near the anterior end, nerves running anteriorly toward sensory or holdfast organs and longitudinal nerve trunks extending posteriorly to near the end of the body. Although variable in number, most trunks are lateral and are connected by transverse commissures. Sensory structures are abundant and are often arranged in species-specific patterns.
In trematodes, the digestive system is usually a blind sac. A mouth is usually found near the anterior end and a muscular pharynx is usually behind the mouth and is used to suck in food. The gut can be saclike or highly branched, but an anus is usually absent. Extracellular digestion is the rule and phagocytosis by the gut epithelium takes substances into the cells. Wastes are eliminated through the mouth. No digestive system is found in cestodes.
The flame cell or protonephridium is the functional unit of the platyhelminth excretory system (See Figure 20.16). The flame cell is a single cell with a flagellar tuft extending into a fine tubule cell. Excess water laden with nitrogenous wastes is forced into the tubule, which joins with other tubules to eventually be eliminated through one or more excretory pores. The excreta are mainly excess water hence some authorities consider the system to be an osmoregulatory system first and excretory system second. In some species, an excretory bladder is just inside the pore.
Reproductive systems have a basic pattern within the phylum, but many variations are found. Most species are monoecious with a few dioecious species found. The reproductive organs are critically important for identifying species. Self-fertilization is possible in the monoecious species, but cross-fertilization is also used. Some cestodes practice hypodermic impregnation which involves sperm transfer through piercing the body wall with a male organ (cirrus) and injecting sperm into the parenchyma of the recipient. It is not known how the sperm find their way to the female system. Most worms deposit the sperm directly into the female tract. Most young are born within an egg membrane, but viviparity and ovoviviparity are also found. In parasitic species the egg is supplied with yolk by non-ovum cells and thus the eggs are considered to be ectolecithal. Asexual reproduction is common for various stages of the trematodes and some cestodes.
Classification of Platyhelminthes (see pp. 192-193 and specific chapters in Roberts & Janovy)
Keep in mind that these taxa are subject to change and reflect the views of some, but not all, parasitologists. We will focus on the parasitic groups. Also note that the classification scheme on pp 189-192 will differ from that found in the specific chapters for several groups. This can be confusing, so I've tried to synthesize things where I could.
Phylum Platyhelminthes
Class Cestoidea
Introduction
These worms are parasites of molluscs primarily, but some are found in turtles and fishes. Other names given this group are Aspidogastrea and Aspidocotylea. There are no economically or medically important members of this group and, therefore, they have not received as much attention as other parasitic groups. However, they seem to represent a link between parasitic and free-living organisms which makes them of more than passing interest.
Body Form
These worms exhibit some fascinating morphological modifications as can be seen in Figure 14.1. One group, the family Aspidogastridae, have a large ventral sucker extending most of the length of the body. This sucker is also known as an opisthaptor and it possesses muscular septa in longitudinal and transverse rows which divide the sucker into shallow loculi or alveoli. The shape, number and arrangement of these structures are taxonomically important. Marginal bodies which are secretory in nature are found between the marginal loculi.
The family Stichocotylidae there are individual suckers (Figure 14.13) arranged in longitudinal series in place of a complex of loculi. In the family Rugogastridae, the ventral sucker is made up of transverse ridges called rugae not unlike the rugae of the human stomach.
The Aspidogastrea possess a longitudinal septum which consists of a layer of connective tissue and muscle arranged horizontally. It divides the body into dorsal and ventral portions and may help the organism cope with the tremendous pressures exerted by contraction of the ventral sucker.
Tegument
The tegument is similar to the general trematode tegument. It is syncytial with an outer layer of distal cytoplasm containing mitochondria and various types of vesicles. Cytons contain the nuclei internal to the superficial muscle layer and communicate with the distal cytoplasm by internuncial processes. Cytons are packed with Golgi complexes. A mucoid layer is found on the outer membrane surface which may have riblike elevations to support the mucus.
Digestive System
A simple digestive tract is found with either a funnel-like mouth or a mouth surrounded by a muscular sucker or several muscular lobes. A muscular pharynx is found at the base of the mouth funnel. The intestine is also known as the cecum, and is a simple sac that reaches the posterior of the body. Lamellae on the mucosal surface of the intestine apparently increase the absorptive surface area. Usually both circular and longitudinal muscles surround the intestine.
Osmoregulatory System
Flame cell protonephridia are connected to numerous capillaries that feed into larger excretory ducts that, in turn, feed into an excretory bladder at the posterior of the body. The small capillaries have many microvilli projecting into their lumens, while the larger ducts have lamellar projections on the surface membranes. These various structures probably have a secretory-absorptive function. There is usually a single excretory pore located dorsosubterminal or terminally.
Nervous System
The nervous system is unusually complex for parasitic worms and is more typical of free-living organisms. A cerebral commissure is located anteriorly and is made up of a complex set of nerves. The peripheral system is a modified ladder type. Many types of sensory receptors have been found among the species and are mostly around the mouth or along the margins of the ventral disk.
The ventral disk and alveoli have a complex system of connecting nerves and commissures that suggest a great deal of neuromuscular coordination. Nerve plexuses are associated with the septum, prepharynx, pharynx, cirrus pouch, uterus, and genital and excretory openings. Some cells in the system may have neurosecretory function.
Reproductive System
The female reproductive system can be seen in Figure 14.6 and consists of an ovary, vitelline cells, uterus, and associated ducts. The ovary is either smooth or lobed and empties into the oviduct. The oviduct empties into the ootype, which is surrounded by Mehlis' gland cells (Figure 14.11). The oviduct has septa and is ciliated. Laurer's canal leads from the ootype and is a short tube that ends blindly in the parenchyma or may connect to the excretory duct. It is probably a vestigial vagina. The vitelline follicles occur in two lateral fields, each of which has a main vitelline duct that fuses with the duct from the other field to form the small vitelline reservoir. The vitelline reservoir empties into the ootype. The uterus extends from the ootype to the genital atrium and usually has a posterior loop and anterior stem. The distal end of the uterus is very muscular and is called the metraterm. It propels the eggs out of the system.
The male reproductive system is similar to that of the Digeneans (Figures 15.2 & 15.5). Testes may be single, double, or multiple and are located posterior to the ovary (Figure 14.6). A vas deferens expands to form an external seminal vesicle that enters the cirrus pouch to become the ejaculatory duct. Some species lack the cirrus pouch. The cirrus pouch opens through the genital pore into a common genital atrium, located on the midventral surface anterior to the leading margin of the ventral disk. The axonemes of the spermatozoon filament have the typical 9 plus 1 structure of microtubules seen in other flatworms (Figure 14.9).
Some aspidobothreans may self-fertilize and the cirrus can deposit sperm in the terminal end of the uterus, which serves as the vagina.
Development and Life Cycles
The eggs of aspidobothreans are ectolecithal; most of the embryo's yolk supply is packaged within separate cells within eggs. After fertilization, the zygotes within their eggshells pass from the parent into the environment. In some species, embryonation is complete before the eggs pass into the environment and the young hatch within a few hours. In other species, several weeks of embryonation in the environment may be required prior to hatching. The larval form is called a cotylocidium (cotylocidia, pl.) (Figure 14.12) and has tufts of cilia that are used for swimming. The larvae possess a mouth, pharynx, simple gut, and prominent posterior-ventral disk lacking alveoli. Alveoli form, tier by tier, as the worm develops. The larval tegument is similar to that of the adult and has a distal cytoplasmic, syncytial layer at the surface with internal cytons.
The life cycle is usually direct and requires no intermediate host. However, aspidobothreans that parasitize vertebrates appear to require an intermediate host. Individual worms can be removed from their hosts and survive several days in water or saline. This suggests that they have a generalized physiology and they are not highly specialized for parasitism. They can even live in the intestines of fishes and turtles if they are eaten by these. Some species can mature in both clams and fish and this extreme lack of host specificity is highly unusual in parasitic species.
Representative Life Cycle
Aspidogaster conchicola
This species is widespread and has been found in freshwater clams in Africa, Europe, and North America. It infects the pericardial cavity of the clams. It has also been found in other mollusk, fishes, and turtles. Adults are 2.5 to 3.0 mm long by 1.0 mm wide (Figure 14.6); oval in shape with a long, mobile neck with a buccal funnel at the end. The loculi on the ventral sucker are arranged in longitudinal rows and total 64 to 66.
Eggs that hatch within the mollusk can develop directly without further migration. If the egg or cotylocidium leaves the mollusk and is drawn into the incurrent siphon of the same or another mollusk, it will reach the nephridiopore and migrate through the kidney into the pericardium. The cotylocidium is 13 to 17 um long at hatching, lacks external cilia, and has a simple posterior sucker lacking loculi. Growth and metamorphosis occur rapidly.
Phylogeny
At first glance, the Aspidobothrea appear to be a link from the Monogenea
to the Digenea, since they share features with each of those two groups.
They differ morphologically from each of the other groups in that the ventral
sucker develops as a new structure, unrelated to any homologue in larvae or
adults of the other groups. The frontal septum in aspidobothreans is
not found in either of the other groups; nor is the septate, ciliated oviduct.
These differences are sufficient for systematists to categorize these organisms
in their own group. They do share some characteristics with each group.
For example, the anatomy is similar to digeneans, the predominance of mollusk
hosts, the presence of Laurer's canal, and a highly developed nervous system
are similar to digeneans. The generalized physiology and saclike cecum
are similar to monogeneans. Many modern systematists place the aspidobothreans
as a sister group of the digeneans.
Digeneans
Introduction
Digenetic trematodes (flukes) are very common parasites that infect all classes of vertebrates. Nearly every organ of the vertebrate body can serve as an infection site for one or more larval or adult digeneans. Digenean life cycles involve at least two hosts and occasionally as many as four hosts. The first intermediate host is usually a mollusk or, rarely, an annelid. Second intermediate hosts are usually invertebrates and occasionally vertebrates. If there is a third intermediate host it is usually a vertebrate. The adult worms usually utilize vertebrates as the definitive host; although their can be exceptions to this. Digeneans can cause economic damage through infection of livestock and many digeneans are of medical importance to humans.
A generalized digenean life cycle is as follows: The first larval stage is the free-swimming, ciliated miracidium (miracidia, pl.) that hatches from its shell and penetrates the first intermediate host, usually a snail and occasionally a different mollusk. The miracidium will shed its epithelium after penetration and change into a simple, saclike sporocyst. Rediae (redia, sing.) develop within the sporocyst asexually. Rediae are more developed than sporocysts possessing a pharynx and gut, not seen in the previous stages. Asexual reproduction within the rediae leads to formation of the next larvae, the cercariae (cercaria, sing.). Cercariae emerge from the snail and usually possess a tail to aid in swimming. Cercariae are considered to be juveniles possessing organs that will develop into adult structures such as genital primordia, suckers, and a digestive tract. A metacercaria (metacercariae, pl.) is found in many species and is required for further development. Metacercariae are often encysted within a second intermediate host. The fully developed metacercaria is infective to the definitive host. When ingested, it will develop into the adult worm.
Body Form
Flukes are often leaflike in form and a great deal of variety in size and shape is seen within the group. The smallest species (Levinsiella minuta) is only 0.16 mm in length and the largest (Fascioloides magna) can be 5.7 cm long and 2.5 cm wide. Adult flukes are dorsoventrally flattened and generally oval in shape, but some are as thick as they are wide. Other species may be round or wider than long. Most flukes have a powerful oral sucker around the mouth and most have a midventral acetabulum or ventral sucker. In the past the terms monostome, distome, and amphistome had taxonomic significance with reference to the number and location of the the suckers. The terms are now used in a descriptive manner although stoma is derived from the Greek and more properly refers to the mouth, not the suckers. However, the terms have remained in common usage as follows: A worm with only an oral sucker is called a monostome (Figure 15.1). A worm with an oral sucker and the acetabulum at the posterior end of the body is called an amphistome (Figure 15.2). A worm with an oral sucker and the acetabulum in some other position is called a distome (Figure 15.3). Modifications around the oral sucker are numerous. In Bunodera, the oral sucker has muscular lappets (Figure 15.4). In Bucephalus, the oral sucker is modified as a holdfast organ with tentacles (Figure 15.5). In Rhopalius spp., a retractable, spiny proboscis is found on either side of the oral sucker (Figure 15.6). Other terms are used to describe digeneans. The echinostomes have a collar of spines around the sucker (Figure 17.1). Holostomes have a forebody and hindbody (Figure 16.1). Schistosomes refer to species of digeneans that usually have separate sexes whereas most digeneans are hermaphroditic. They are also unusual in that they lack a second intermediate host and mature in the blood vessels of their definitive hosts. During the course of the semester you will encounter other descriptive terms for parasites, be sure to use your glossary or other resources to help you define these terms.
Tegument
The tegument is a living, complex tissue. The epidermis is "sunken"; that is, it is a distal anucleate layer (distal cytoplasm). The cell bodies containing the nuclei (cytons) lie beneath a superficial layer of muscle It is syncytial with an outer layer of distal cytoplasm containing mitochondria and various types of vesicles. Cytons contain the nuclei internal to the superficial muscle layer and communicate with the distal cytoplasm by internuncial processes (Figure 15.7). The tegument is considered to be syncytial because the cytoplasm is continuous with no intervening cell membranes. The general organization is the same as that found in the cestodes, but differs in detail and one individual may have significant differences from one part of the body to the next. Various species have spines, bosses (raised, rounded areas), papillae, and other modifications on the tegument (Figures 15.8, 15.9 & 15.10).
Golgi-derived vesicles are usually found in the distal cytoplasm, but their function is unknown in most species. However, in Schistosoma mansoni the vesicles help renew the surface membrane by continuously moving outward through the distal cytoplasm. The vesicles might replace membrane damaged by host antibodies. Mitochondria are also found in the distal cytoplasm of most species that have been examined.
The tegument of adult trematodes is not modified with microvilluslike structures that increase absorptive surface area, but some species have deep pits and channels that may serve that purpose (Figure 15.9).
The tegument in larval forms varies. Miracidia of some species are covered with ciliated epithelial cells interrupted by intercellular ridges (Figure 15.11). When the miracidia changes into a sporocyst, the ciliated epithelium is lost and the distal cytoplasm spreads over the surface of the worm. Sporocysts and rediae are covered with well-developed microvilli. The luminal surface of the tegumental cells in the redia may be thrown into a large number of flattened sheets that extend to the other cells in the body wall and to the cercarial embryos contained in the lumen. Nutrient molecules can pass through the tegument to the developing cercariae. The cercarial tegument changes as it develops (Figure 15.12). Early on, the embryos are covered with a primary epidermis below which a definitive epithelium forms. The nuclei of this secondary epithelium sink into the parenchyma resulting in a cercarial tegument that is similar to that of the adult. Cystogenic cells in the parenchyma begin to secrete cyst material that passes into the distal cytoplasm of the tegument. When the cercarial tegument sloughs off, the cyst material within changes chemically and/or physically to envelop the worm in a cyst (metacercarial cyst). Following this, the cystogenic cells in the parenchyma flow toward the surface and a thin layer of cytoplasm spreads over the organism to become the final adult tegument. The overall processes may vary somewhat from species to species.
The adult tegument is interrupted by cytoplasmic projections of gland cells, by nerve endings, and by excretory pore openings. The teguments of miracidia and cercariae may have penetrations glands that open at the anterior, and some adults have glandular organs opening to the exterior.
Muscular System
In most digeneans, superficial muscle layers can be found that consist of circular, longitudinal, and diagonal layers around the body and below the distal cytoplasm of the tegument. The degree of muscularization varies markedly within the digeneans from feeble to extremely strong and everything in between. Muscles may be more prominent in the anterior parts of the body, and strands connecting the dorsal muscles to the ventral muscles can be found in the lateral parts of the worm. Muscle cells are smooth with nuclei in cytons called myoblasts. The suckers and pharynx often have well-developed radial muscle fibers. The intestinal ceca are often surrounded by a network of fibers that probably helps to fill and empty them.
Digestive System
The digestive tracts will vary with the nutrient type and habitat within the host. Depending on the means of feeding, one or more components of the basic flatworm digestive tract may be missing. In general, flukes found in the lungs, intestine, urinary bladder, rectum, and bile duct of the host feed by taking in blood, mucosa, or other tissue. For example, some lung flukes will draw tissue into their oral sucker and erode the tissue with strong contractions of the pharyngeal muscles. Blood will then be consumed from the capillaries. In species that lack a pharynx, the esophageal muscles are quite strong and the esophagus serves the function of the pharynx. S. mansoni is bathed by the nutritive blood it lives in and lacks both an esophagus and pharynx.
In most species, digestion of foods occurs extracellularly in the ceca. However, Fasciola hepatica utilizes both intracellular and extracellular processes. Species that feed on blood have a particular problem in coping with the iron of the hemoglobin molecule. Some species expel the iron through the excretory system and tegument, other species bind it tightly to protein and store it in cells, still other species produce insoluble end products within the cecal lumen that are periodically regurgitated.
Various digestive enzymes have been found in trematodes apparently secreted by the gastrodermal cells rather than specific gland cells. Some of the enzymes found include: Proteases, a dipeptidase, an aminopeptidase, lipases, acid and alkaline phosphatases, and esterases.
Microvilli have been found on the membranes of gastrodermal cells in all species examined. The microvilli are arranged as a brush border that increases the absorptive surface area of the cells, similar to what is found in many species of animals, including humans. Cytoplasmic processes may also project from the gastrodermal cells (Figure 15.16). These can be short and irregular to long and extend into the lumen.
Absorption can also occur across the teguments, especially for small nutrient molecules. For example, in the species examined, glucose was absorbed across the tegument and not via the gut. The ability to absorb other nutrients across the tegument or via the gut varies markedly among species. However, species that do utilize tegument absorption, possess large numbers of tegumental mitochondria to provide energy for the active transport of the nutrients.
Excretory & Osmoregulatory System
The excretory systems of digeneans serve both excretory and osmoregulatory functions. Metabolic wastes are removed across the tegument and the lining of the gut by diffusion and by exocytosis of vesicles. Wastes are also removed by the excretory system.
Flame bulb protonephridia system is found in the digeneans. A protonephridium is a unit of an excretory system that is closed at proximal end and open at the distal end to a collecting tubule. The flame bulb or cell (Figure 20.15) is flask shaped with a tuft of fused flagella to provide the force to move the fluid within the system. A filtering weir will allow fluids and small molecules into the excretory system and keep larger molecules in the tissues. Beating of the flagella creates a gradient that draws fluid through the weir and into the collecting tubule. Leptotriches may extend from the internal and external surface of the weir and appear to increase filtering by keeping surrounding cells away from the weir and keeping the weir away from the tuft of flagella.
The collecting tubules of the flame bulbs join to form collecting ducts on each side of the worm. The collecting ducts from each side will feed into the excretory bladder. In the adult, the bladder empties out a single pore. In digeneans, the pore is usually located posteriorly. In some species, the walls of the collecting ducts are lined with microvilli suggesting that there is a transfer of substances in or out in these ducts. Freshwater trematodes have better developed protonephridial systems than do marine worms, emphasizing the osmoregulatory function of the system. The free-swimming stages of freshwater trematodes require a very efficient osmoregulatory system to remove water.
The primary nitrogenous waste product in trematodes is ammonia, but some species appear to excrete uric acid or urea.
Nervous System
The nervous system is the typical flatworm ladder (orthogon) type (15.13). Commissures connect a pair of cerebral ganglia in the anterior end of the worm. Three main trunks; dorsal, lateral, and ventral; arise from the ganglia to supply the posterior parts of the body. The ventral branch is the best developed and it is connected by commissures to the other branches. The branches provide motor and sensory endings to muscles and the tegument. Sensory endings are numerous in the anterior end especially around the oral sucker.
Sensory endings in adult digeneans are minimal because this stage requires no orientation to light or gravity. Only one type of sensory ending has been found in adults. It is a bulbous ending in the tegument with a short, modified cilium projecting from it, and the cilium is enclosed along its length by a thin layer of tegument. This receptor type is thought to respond to touch (tangoreceptor).
Miracidia and cercariae have numerous types of sense organs probably related to finding a host quickly before their stored energy supplies are exhausted. In S. mansoni cercariae, uniciliate bulbous endings similar to those seen in adults have been found as well as a bulbous type with a long unsheathed cilium. These cercariae also have small, flask-shaped endings with five or six cilia along their lateral areas (Figure 15.14). These are probably chemosensory in nature.
Another possible chemoreceptor, found in the miracidium of at least one species, consists of two dorsal papillae between ciliated plates. Each papilla is a nerve ending and has a number of modified cilia radiating from it parallel to the surface of the miracidium. The sensory endings are quite similar to the vertebrate olfactory endings.
Cercaria and miracidia often have eyespots, which are thought to help orient these larvae with respect to light. Eyespots present in adults are functionless. The eyespots consist of one or two cup-shaped pigment cells surrounding the parallel rhabdomeric microvilli of one or more retinular cells (Figure 15.15). The cup shape of the pigment cells allows the organism to distinguish light direction.
Neurotransmitters found in digeneans include 5-hydroxytryptamine, and acetyl choline. The former is excitatory, while the latter is inhibitory. Neuropeptides have been found that may serve as messenger systems for regulation and control, but their specific functions remain unknown.
Reproductive System
The typical female reproductive system can be seen in Figure 15.17 and consists of an ovary, vitelline cells, uterus, and associated ducts. The ovary is usually round or oval, but may be lobed or branched. The oviduct is short and has a proximal sphincter called the ovicapt, which controls passage of the ova. The female ducts, including the oviduct, are ciliated. The seminal vesicle is formed from an outpouching of the oviduct. Laurer's canal branches from the base of Laurer's canal and it ends blindly in the parenchyma or opens through the tegument. It is probably a vestigial vagina, but may store sperm in some species. The vitelline follicles occur in two lateral fields, each of which has a main vitelline duct that joins the vitelline reservoir. The common vitelline duct leads away from the vitelline reservoir and joins the oviduct (Figure 15.18). Vitelline glands have a species specific distribution that makes them important in identifying digeneans. The oviduct expands to form the ootype, which is surrounded by numerous unicellular Mehlis' glands. The structure illustrated in Figure 15.18 forms the oogenotop or egg-forming apparatus. The duct expands to form the uterus after the ootype, and this structure extends to the genital pore. The uterus may be short and straight, or long and coiled. The distal end of the uterus is very muscular and is called the metraterm. It propels the eggs out of the system and serves as a vagina. Both the female and male genital pores open near each other, usually in a genital atrium. In some species, the genital atrium is surrounded by a muscular sucker called the gonotyl.
Similar to what is seen in other animals, including humans, the germ cells that leave the ovary have not completed meiosis and are not true ova but are oocytes. Meiosis is completed after sperm penetration. Only after meiosis is complete, will the female and male pronuclei fuse.
Each oocytes that leaves the ovary becomes associated with several vitelline cells and a sperm as it passes down the oviduct. These all conjoin in the ootype along with the secretions of the Mehlis' glands. In the past, the Mehlis' glands were though to contribute to the eggshell, but it is now known that the vitelline cells contribute most of the shell and the function of the Mehlis' glands' secretions are unclear. Perhaps the Mehlis' glands' secretions serve as an eggshell template.
The eggshell is hardened and stabilized through the quinone-tanning process of sclerotization. The known structural proteins include keratin, sclerotin, resilin, and elastin. These are stabilized during eggshell formation by crosslinkage of amino acid moieties in adjacent protein chains.
In the male reproductive system is the testes are usually double, but may single or multiple and are located posterior to the ovary (Figure 15.17). Testes can be round to highly branched depending on species. Each testis has a vas efferens that joins with the other vas efferens to form the vas deferens. The vas deferens travels to the genital pore, which is usually in a genital atrium located midventrally anterior to the acetabulum. However, the location of the genital atrium can be quite variable. Usually the vas deferens enters a muscular cirrus pouch before reaching the genital atrium and it often expands into an internal seminal vesicle. After the seminal vesicle, the duct constricts to form a thin ejaculatory duct that extends the the rest of the length of the cirrus pouch and forms a muscular cirrus (penislike organ) at its distal end. The cirrus can be invaginated into the cirrus pouch and evaginated for transfer of sperm to the female system. The cirrus may be covered with spines or naked. Prostate gland cells usually surround the ejaculatory duct and a muscular pars prostatica is found in some species. Some species are capable of self-fertilization.
A great deal of variation in the terminal organs occurs among species of digeneans. In some species the cirrus pouch and prostate gland are absent and the vas deferens is expanded into a muscular seminal vesicle. In other species, the vas deferens expands into an external seminal vesicle prior to reaching the cirrus pouch.
Development
Typically, at least two hosts are required to complete the life cycle of digeneans. Usually a vertebrate is the definitive host in which sexual reproduction occurs and a mollusk serves for one or more generations of asexual reproduction (intermediate host). Rarely, annelids serve as the intermediate host.
The variability and complexity in this alternation of sexual and asexual generations are tremendous. In fact, many digenean life cycles have never been worked out. Up to six different body forms (not counting the egg) have been recognized in digenean life cycles and within a given species, certain stages may be repeated during ontogeny, while stages found in other species may be absent. For example, some species have two generations of rediae. Too many variations on exist to make sweeping generalizations about life cycles. However, the following description covers most of the general information.
Embryogenesis
In both sexual and asexual reproduction, the first cleavage produces a propagatory cell (stem cell) and a somatic cell. These cells are cytologically indistinguishable. Cells that arise from the somatic cell will give rise to the body tissues of the embryo, whether miradicium, sporocyst, redia, or cercaria. The propagatory cell may produce another propagatory cell and somatic cell, but eventually the propagatory cell cleavages will produce only more propagatory cells. At this point, each propagatory cell will become an additional embryo in the miracidium, sporocyst, or redia. In the cercaria, the propagatory cells will become gonad primordia, the forerunners of the ovary and testes. Hence, the propagatory cells are the germinal cells in the asexual stages of reproduction, and give rise to the germ cells of the sexual adult worm. If a sporocyst stage is missing in a life cycle, the redial embryos will develop in the miracidium to be released after penetration of the host. The youngest developing embryos in any stage are usually seen in the posterior portions of the body and are often referred to as germ balls.
Larval and Juvenile Development- the Egg (Shelled Embryo)
The "egg" of a digenean contains a developing or developed embryo enclosed within its capsule or shell. Most fluke eggshells have an operculum at one end and the larva eventually is released through this. Blood fluke eggshells lack an operculum. Significant variation exists in the size, shape, thickness, and color of digenean eggs. Some eggs can be used diagnostically to identify infections through stool samples.
The egg may contain an embryo that has undergone only a few cleavages when released and further embryonation occurs in response to environmental cues. Other species have a fully developed miracidium in the egg that is released soon after the egg leaves the adult. Eggs that embryonate in the environment require water to prevent desiccation, which occurs rapidly in the absence of water. High oxygen tension stimulates embryonation, but many eggs can remain viable for long periods of time at low oxygen tensions. Some species require a specific pH range for embryonation. Temperature is a critical factor for embryonation. Within physiological constraints, developmental time will vary directly with temperature, slower at low temperature, faster at higher temperatures. However, above 30 C development in many species will slow and in most will stop at about 37 C. Freezing will kill eggs rapidly. Light may also influence development, but to what extent is not known.
Some species hatch in water, while other hatch only after being eaten by a suitable intermediate host. For species that hatch in water, light and osmotic pressure are important in stimulation of hatching. Osmotic pressure, carbon dioxide tension, and host enzymatic activity probably stimulate hatching in those species that are consumed by an intermediate host. The hatching of some species seems to be timed to coincide with the movements of intermediate hosts, so that the miracidia are released when the mollusk host is nearby.
Miracidium
Figure 15.19 presents a typical miracidium. They can easily be mistaken for protozoa because of their diminutive size and ciliated epithelium. Most miracidia are piriform and have a retractable apical papilla anteriorly. The papilla has five pairs of duct openings from glands and two pairs of sensory nerve endings (Figure 15.20). The glands are penetration glands. Apical glands are quite noticeable just below the papilla (Figure 15.20). The apical gland is thought to secrete histolytic enzymes that help the miracidium penetrate its next host. The sensory endings eventually connect to a large ganglion within the miracidium.
The number and shape of the cilia covering the miracidium are species-specific. Beneath the epithelium are circular and longitudinal muscles. Some species lack cilia, while others have them arranged in ciliated bars. There may be one or two pairs of protonephridia connected to excretory pores in the posterolateral part of the miracidium.
The posterior portion of the miracidium also contains the propagatory cells mentioned earlier.
The free-swimming miracidia must move rapidly to find an intermediate host, because their energy reserves are used up in a matter of hours. It has been found that snail mucus is a strong attractant for many miracidia. Once in contact with a snail or other appropriate mollusk, the apical papilla attaches to the host, actively contracting and extending like an auger. Tissue cytolysis occurs as the miracidium penetrates. The ciliated epithelium is sloughed off and penetration is usually complete within 30 minutes. Miracidia that are eaten by their snail hosts, will not hatch until they have entered the snail's gut.
Sporocyst
The sporocyst is quite different than the miracidium and significant changes occur after the miracidium penetrates. A new tegument with microvilli forms; the miracidial subtegumental muscle layer and protonephridial system are maintained, but the other miracidial structures disappear. Nutrients are absorbed through the tegument, since there is no mouth or digestive system. A sporocyst is little more than a nutrient absorbing sac for development of the next larval stage. Hence, miracidia, sporocysts, and rediae are sometimes referred as germinal sacs. Sporocysts can be found in almost any tissue, but are often near the foot, antennae, or gills. A generation of daughter sporocysts may form, while in other species rediae form, and in yet other species, cercariae form directly (Figure 15.21).
One species of digenean, Leucochloridium paradoxum, has a particularly unique sporocyst. Its sporocyst is modified so that a broodsac lies in the head-foot of the snail and enters the tentacles. In the tentacular component of the broodsac, the embryos mature into cercariae. During the process, the broodsac enlarges, becomes brightly colored, and pulsates rapidly. This makes the snail quite visible to birds which feed on the snails and serve as the definitive host for the parasite. It is one of many modifications that parasites make to their hosts to enhance transmission to the next host.
Redia
Figure 15.22 illustrates a redia with additional embryos developing within. Rediae leave the sporocyst and usually migrate to the hepatopancreas or gonad of the molluscan host. Rediae tend to be elongate with a blunt posterior end. Stumpy appendages called procrusculi may be present. They can crawl about within the host and have a simple digestive tract with a mouth, muscular pharynx, and short gut. The pharyngeal muscles serve to pump food as seen in the adults. They feed on host tissues and sporocysts of their own or other species. The absorptive surface area of the gut is increased by lamelloid, flattened, or ribbon like processes. The gut cells appear capable of phagocytosis. The tegument also can absorb nutrients and may have microvilli or lamelloid processes.
Within the rediae, daughter rediae or cercariae will develop. Cercariae are released through a birth pore. Rediae will produce daughter rediae until the population level reaches a certain threshold at which point the rediae will start to produce cercariae.
Cercaria
The cercaria is a free-swimming form that will infect a vertebrate intermediate or definitive host. It lives for only a short time because it has limited glycogen stores, so it must quickly find its next host. Most cercariae have tails, but the tail is reduced or absent in some species. The cercariae of these species crawl about or are eaten by the next host. In some cases, the cercariae do not even leave the sporocyst or redia prior to being eaten by the next host. As Figure 15.23 illustrates, there are many morphological forms of cercariae.
The ease with which cercariae can be collected and prepared for examination has made them a well-studied stage in digenean life cycles. The morphology can be used to help differentiate among different species more easily than can be done for adults, in many cases. In fact, the adult form may not be known and the name Cercaria can be used as a proper genus name until the full life cycle is worked out.
The typical cercaria has an anterior mouth surrounded by an oral sucker, although in some species the mouth is midventral. A prepharynx, muscular pharynx and forked intestine are also found. Many cercariae have a variety of glands near the anterior margin and it is assumed that these glands produce secretions to help penetration; hence, the name penetration glands. Schistosome cercariae have at least four types of glands:
1. Escape Glands- The contents of these glands are expelled during release of the cercaria from the mollusk, but their actual function is unknown.
2. Head Gland- The secretion from this gland is added to the matrix of the tegument and is thought to help the schistosomule adjust after penetration.
3. Postacetabular Glands- These glands produce mucus and are known to help the cercaria adhere to surfaces.
4. Preacetabular Glands- The secretions contain calcium and a variety of enzymes. These secretions seem to help the cercaria penetrate the next host.
Cystogenic gland cells are very prominent in cercariae that will encyst on vegetation or other objects, such as Fasciola hepatica.
Many morphological features are found to be unique to species or larger taxa of cercariae and can be important in identifying these organisms. Many terms are used to describe these features, such as xiphidiocercaria (possess a stylet in the anterior margin of the oral sucker), cercariaeum (without a tail), microcercous cercaria (with a small, knoblike tail), furcocercous cercaria (with a forked tail), and ophthalmocercaria (has eyespots). If a cercaria possesses more than one of the above traits, the terms might be combined. For example, an ophthalmoxiphidiocercaria has eyespots and a stylet in the oral sucker. We have examples of many of these cercariae in the snails and clams found in the marsh on campus.
Cercariae have a well-developed excretory system and, in some species, the excretory bladder empties out of one or two pores in the tail. The number and arrangement of the protonephridia are constant in a species and have been used extensively in species identification. Regardless of the number of flame cells, each one has a small capillary duct that joins with the ducts from other flame cells to form an accessory duct. The accessory ducts join the anterior or posterior collecting ducts, and these, in turn, join to form the common collecting duct on each side of the cercaria. These structures are illustrated in Figure 15.24. A mesostomate arrangement occurs when the common collecting ducts extend to the region of the midbody and then fuse with the excretory bladder (vesicle). A stenostomate cercaria will have the common collecting ducts extend to the anterior before passing to the posterior to join the bladder. A standard flame cell formula has been developed to express the number and arrangement of the flame cells. For example, 2[(3+3)(3+3)] means that both sides (2) of the cercaria have three flame cells on each of two accessory tubules (3+3) on the anterior collecting duct, plus the same arrangement on the posterior collecting duct (3+3). The cercaria in Figure 23.14 has a formula of 2[(3+3+3)(3+3+3)].
Cercariae exhibit many adaptations designed to help them locate the next host. Most are active swimmers and seem to rely on chance in contacting the host. Some species are photopositive, first dispersing to the surface, and then becoming photonegative to return to the bottom where the next host is located. Some cercariae remain quiescent on the bottom until a fish swims over casting a shadow at which point the cercariae become active and swim upward. Some species quit swimming when in a current so that they can be drawn across the the gills of a crustacean host, where they attach and penetrate. Some cercariae are large and pigmented and appear to be food items to fish which eat them. Some cercariae unite in clusters. Some cercariae float to encounter their hosts. Schistosoma mansoni cercariae are attracted to a thermal gradient such as would be created around a human wading in the water. Halipegus spp. have a cystophorous cercaria with the body withdrawn into the tail, which serves as an injection device. The second intermediate host in the life cycle is a copepod crustacean that eats the caudal cyst containing the cercaria. The mandibles of the copepod break the cyst and a delivery tube is rapidly everted into the mouth of the copepod, piercing the midgut, and allowing the cercaria to pass through the tube into the hemocoel of the copepod. We have at least one species of Halipegus in the marsh on campus and hopefully we will be able to find these cercariae.
Mesocercaria
In the genus Alaria, a unique larval form called a mesocercaria is found. It is intermediate between the cercaria and metacercaria (Figure 16.3).
Metacercaria
In many species of digenean, a quiescent stage called the metacercaria exists. Blood flukes lack this stage. The metacercaria is usually encysted, but in some species it is not. Most metacercaria are found on or in an intermediate host, but some encyst on vegetation, sticks, rocks, or even free in the water.
The cercaria will shed its tail at the start of encystment. The process is most complex in species that encyst on inanimate objects or plants. Fasciola hepatica encysts on plants and has several different types of cystogenic cells producing secretions for cyst construction. Metacercariae that encyst in intermediate hosts have thinner, simpler cyst walls and the host usually contributes some components to the cyst wall.
Development of the metacercaria to the infective stage will vary markedly among many species. Species that encyst on vegetation or inanimate objects are infective almost immediately to the definitive host. These species live on stored food and must quickly infect a host. Some species require at least several days of physiological change within an intermediate host to become infective. Still other species undergo growth and metamorphosis and then enter a resting stage in which they are infective. These species can require several weeks to become infective. The species in intermediate hosts can usually obtain some nutrients from the host and are able to survive longer than those in the first group. Some metacercaria in intermediate hosts have been found to remain viable for up to 7 years. Regardless, whether the quiescent stage is long or short, it is during this time that the parasite is infective to the definitive host.
The metacercarial stage is a highly adaptive stage because it allows for transmission to definitive hosts that do not feed on first intermediate hosts, or may not be present in the same environment as the first intermediate host. The metacercaria can also serve as a survival mechanism during unfavorable periods, such as when a definitive host is absent on a seasonal basis.
Development in the Definitive Host
Some digeneans are almost mature when they infect the definitive host because they have undergone extensive development as metacercaria and little further development is needed. At the other extreme, the schistosomes must undergo extensive development, morphological change, and maturation in the definitive host because they lack a metacercaria. A few species reach sexual maturity in the mollusk host and lack a vertebrate definitive host. Some species reach sexual maturity in another invertebrate host. On this campus, Allocreadium neotenicum matures within an isopod or amphipod crustacean host. We will try to find these in April.
In most species, for development to occur in the definitive host, excystation must take place first. The more structurally complex the metacercarial cyst, the more complex the stimuli needed to initiate excystation. For example, F. hepatica has its outer cyst removed by digestive enzymes of the host, but escape from the inner cyst require the presence of a temperature of 39 C, low oxidation-reduction potential, carbon dioxide, and bile. These conditions will usually be found only in the gut of the definitive host, and this helps to prevent excystation in an unsuitable environment. Those metacercariae with only a thin cyst can usually escape in response to host enzymes alone, although some species escape more quickly if bile salts are also present.
After excystation, the worm must migrate to its final site. The site may be in the intestine, lungs, liver, or circulatory system. Those in the intestine have the shortest migration. Access to the liver is usually via the bile duct. However, F. hepatica burrows through the gut wall into the peritoneal cavity and wanders around until it encounters the liver. Access to the lungs may be gained after migration through the gut wall into the peritoneal cavity, through the diaphragm, and finally into the lungs.
Hazards and Barriers to Transmission
Excluding for now the obvious impediments posed by the defense and immune systems of hosts, ponder the various physical, chemical, and physiological barriers the various life cycle stages must overcome to infect the intermediate and definitive hosts in the life cycle.
The miracidium will be released into a freshwater or seawater environment with a different osmotic pressure regime than that in the definitive host. It must be able to withstand the potentially drastic differences until a mollusk host is encountered. The mollusk poses quite different physiological challenges to the parasite than either the water or vertebrate host. During each transition, the physiology of the worm must be adjusted to handle the new conditions. Again when the worm leaves the mollusk and enters the next host and leaves that host to enter the definitive host, the conditions will be quite varied. Consider that a cercaria may enter an ectothermic fish second intermediate host in which develops the metacercaria. The definitive host may be an endothermic vertebrate that provides a markedly different environment from the fish.
Penetration of a definitive host by a cercaria of a blood fluke can be a very hazardous time. The skin of the host is a formidable barrier and over 90% of the stored energy of the cercaria is used up in this process. Having penetrated, the schistosomule must deal with the host's immune and nonspecific defense mechanisms. The osmotic pressure will be quite different in the human compared with water or the snail from which the cercaria was released. To handle these variabilities, the osmoregulatory system must be able to take in or remove water as conditions change. The tegument also seems to change its permeability to water depending on the environment the cercaria is in. For most species, the types of changes that occur are poorly understood.
Cercarial attraction to hosts has been found to be mediated by a variety of host-produced compounds that serve as chemoattractants. Once attracted to the host, still other host-produced compounds can serve to stimulate penetration.
Summary of Life Cycles
Figure 15.25 illustrates variations on the theme of digenean life cycles for 8 species of parasite. The generalized life cycle includes the egg, miracidium, sporocyst, redia, cercaria, metacercaria, and adult. However, as you can see from the figure, exceptions are the rule.
Metabolism
Although the metabolism of some species of adult trematodes have been well-studied, little is known about the metabolism of larval stages. The best studied species tend to be those of medical or economic importance.
A glycolytic pathway is present and most trematodes are facultative anaerobes. However, components of a Krebs cycle are also present even though most trematodes do not utilize this pathway to the fullest extent and much of the potential energy of the glucose molecule is not harvested.
Fasciola hepatica has all of the enzymes necessary for operation of Krebs cycle, but the activity of two of the enzymes is very low, but some additional energy is gained through these pathways (Figure 15.26). Schistosomes seem to have the ability to utilize Krebs cycle the electron and gain that additional ATP available from these reactions sequences.
Digeneans utilize glycogen as their main energy storage compound. Depending on the species, from 9% to 30% of the dry weight is glycogen. S. mansoni females are an exception to this at only 3.5% of dry weight. The availability of food makes it surprising that trematodes store so much glycogen as adults. However, if starvation conditions occur, the high amount glycogen available would help the worm get through until food is available again.
Although few species have been studied, the metabolism of the free-swimming miracidia and cercariae appears to be aerobic, which is not surprising in that they would need to obtain every possible ATP they could from each glucose molecule that is metabolized. The sporocysts apparently have metabolic processes similar to adults, but it is difficult to study them as they are intimately associated with their host tissues.
Although lipids are found in trematodes, there is no evidence that they are used as energy storage compounds are in energy metabolism.
Nitrogenous waste products from the species studied are ammonia and urea as well as some amino acids.
Phylogeny
Currently, most systematists believe that trematodes share an ancestor with some of the free-living flatworms. Regardless of their origin, it is a difficult task to explain the complexity of trematode life cycles in terms of natural selection.
One scenario is that a free-living developmental stage of a digenean ancestor invaded a mollusk and started feeding on its tissues. This is supported first by the fact that digeneans show much more host specificity for their molluscan host than for their vertebrate host. Secondly, the known endocommensal flatworms utilize mollusks and echinoderms as their main hosts. As the parasitic relationship developed over time, asexual reproduction could have evolved and this would have also been advantageous to the parasite. The free-living adult might have then been eaten by a fish, and any individuals that could survive the fish digestive tract could establish a parasitic life style. In both cases, parasitism provides a selective advantage for reproduction in that fewer resources are needed for maintenance and survival and more resources can be put into reproduction. More offspring are then produced, increasing the fitness of the individual worm.
Another factor that suggests that the ancestral digenean adult was free-living is the requirement that the worm leave the snail host to infect the next host. It is incapable of infecting the definitive host while still in the first intermediate host and the first intermediate host cannot also serve as the definitive host.
The miracidium appears to represent a larval form of the ancestral digenean because all species still have them in the life cycle.
Once a two-host life cycle was established further elaborations occurred to bring in additional intermediate hosts when they provided a selective advantage. For example, the metacercariae can serve for protection as well as a stage for development to the stage that infects the definitive host.
It is thought that digeneans adapted to vertebrate relatively recently. This is bolstered by the fact that are very few species of digeneans in the Chondrichthyes, an evolutionarily old class of vertebrates, while more modern vertebrate classes are infected with many trematode species. Urea is commonly found in the tissues of the Chondrichthyes, but not in the tissues of the more modern vertebrates. The urea is important to the osmoregulation of the sharks and rays. When tested, the urea has been found to be toxic to flukes. This suggests that the osmoregulatory system of the Chondrichthyes evolved before digeneans became parasitic and it now poses a barrier to infection by digeneans. On the other hand, tapeworms are quite common in sharks and rays and they are able to tolerate or degrade the tissue urea.
A cladistic analysis of the relationships among digeneans is illustrated in Figure 15.27.
Monogeneans
Introduction
The organisms in this groups are primarily ectoparasites of fishes. However, a few species are found internally in the stomodeum or proctodeum or in the ureters of fishes and the bladders of turtles and frogs. They are hermaphroditic as are most other flatworms. One species is known from mammals, Oculotrema hippopotami from the eye of the hippopotamus. They usually do not cause mortality in fishes unless overcrowding occurs in the fish population, such as in a fish hatchery.
This is not a well-studied group and probably fewer than half the extant species have been identified to date. Their phylogenetic relationships are still a matter of discussion, but most modern phylogenetic analysis suggest that they are more closely related to the tapeworms than to the trematodes. Note that in the classifications schemes of Roberts and Janovy they have they have two different names for the class that contains these worms, Class Monogenoidea and Class Monogenea. This illustrates the confusing nature of classifying organisms as science provides new molecular techniques that allow us to examine specimens in more detail.
Monogeneans tend to be very host specific and very narrow in their choice of a site on the host. In some cases, one species may live at the tip of a gill filament, while another is found at the base. Some monogeneans remain fixed at their initial site of attachment, while other species can relocate. Some species parasitize only mature fish, while others parasitize only immature fish. The mucus produced by the epidermis of the fish host appears to attract the free-swimming larva for many species. Monogenean species may have life spans of only a few days to several years. They tend to drop off of the host after it dies.
Body Form
The monogeneans possess a unique holdfast device, the opisthaptor, which is located posteriorly. The body segments are the cephalic region (anterior to pharynx), the trunk or body proper, the peduncle (posterior tapering), and the opisthaptor (Figure 19.1). Monogeneans range in size from 0.03 to 20.0 mm long. Marine species tend to be larger than freshwater species. The dorsal aspect of the body is usually convex and the ventral aspect is concave.
A prohaptor is found at the anterior end of the body. It is a collection of adhesive, feeding, and sense organs. In some cases the prohaptor is not connected with the mouth funnel (Figure 19.2) and in other cases it is (Figure 19.3). In the first case, the prohaptor usually has a number of cephalic or head glands, that secrete sticky substances that help the monogenean move. The area may have dense, long microvilli that help spread the substances. Some species have shallow grooves or bothria, which serve as suckers and work in conjunction with the head gland secretions.
The second type of prohaptor has modifications of the mouth and buccal funnel. One type is a simple oral sucker surrounding the mouth. In some species, two buccal organs (buccal suckers) are embedded within the walls of the buccal funnel. These may assist in feeding on the host's blood.
The opisthaptor serves as the holdfast allowing the parasite to remain strongly attached to the fish while the anterior end is used for feeding. The opisthaptor is found as a tiny structure in larval forms that may either develop directly into the adult structure or the adult organ may develop from other sources besides the juvenile opisthaptor. Regardless, there are numerous structures and modifications associated with the opisthaptor among the various monogenean species. One type is muscular with a large disk that has well-developed suckers or shallow loculi. Large hooks or anchors (hamuli) are frequently associated with the opisthaptor. The anchors are usually centrally located in the opisthaptor and occur in one to three pairs. Support of the anchors is provided by connecting bars or accessory sclerites (Figure 19.5).
In addition to anchors, smaller hooks are associated with the opisthaptor. Marginal hooks are tiny hooklets retained from the larval opisthaptor. Central hooks may also be present. They are so small that it is difficult to see them in prepared whole mounts.
Compensating disks or supplementary disks are found near the base of the opisthaptor in one family. They are not part of the opisthaptor, but are accessory to it and are made up of sclerotized lamellae or spines. Suckers may also be found on the ventral surface of the opisthaptor in some species. Finally, clamps are found in many species and serve as pinching devices that aid adherence to the host (Figure 19.6). The clamps may be muscular or sclerotized.
The various combinations of suckers, hooks, clamps, and other opisthaptor structures are important taxonomic features that help to identify the species of monogeneans.
Tegument
The basic structure of the tegument is similar to that of cestodes and digeneans. Review the information on the tegument of the digeneans. The genus Gyrodactylus is unusual in that it seems to lack the trabeculae and cytons observed in other monogeneans as well as the trematodes and cestodes.
Muscular and Nervous Systems
The superficial muscles beneath the tegument consist of circular, diagonal, and longitudinal muscle layers. Other muscles are associated with the opisthaptor and work to assist the adhesive functions of the various kinds of opisthaptors. One type of opisthaptor and its muscles are seen in Figure 19.7.
The nervous system is typical of that found in the digeneans; the ladder type with cerebral ganglia. Review the description of the digenean nervous system. The adhesive organs of the opisthaptor are well-innervated. A variety of sensory organs have been identified in the monogeneans. The larval forms usually have pigmented eyes and many species of adults also have eyes. Several types of ciliary sense organs have been identified in the tegument, which may be touch receptors.
Osmoregulatory System
Monogeneans have the typical flatworm flame cell protonephridium excretory unit. A thin-walled capillary from each protonephridium fuses with a succession of ducts that lead to two lateral excretory pores near the anterior of the worm. There is a contractile bladder associated with each terminal duct. The ultrastructure of the excretory system is similar to that of the digeneans, except that the tubule surface area is increased by strong reticulations of the wall rather than microvilli.
Nutrient Acquisition
Behind the mouth and buccal funnel are a short prepharynx and a muscular and glandular pharynx. These structures serve as a powerful sucking device for drawing food into the worm. The pharyngeal glands secrete powerful proteases for eroding the host's epidermis and the worm then sucks up the lysed products. An esophagus may be behind the pharynx, but in many species it is lacking. Most digeneans have an intestine that divides into two crura that may be highly branched and may rejoin along their lengths. Crura that join near the posterior of the share a common tube from that point on to the posterior of the worm. An anus is lacking. The primary host tissues ingested by monogeneans are mucus and epithelial cells, although some species ingest host blood.
Female Reproductive System
Monogeneans are hermaphroditic and cross-feritilization is common. Monogeneans possess a single ovary (germarium) that is usually anterior to the testes (Figures 19.1 & 19.9). The ovary may be round, oval, elongate, or lobed. The oviduct leaves the ovary and receives the vitelline, vaginal, and genitointestinal ducts as it passes toward the ootype. A seminal receptacle is present as a swelling of the oviduct or a separate sac with a duct connecting to the oviduct. Vitellaria are numerous and often are found throughout the parenchyma and even in the opisthaptor. Each group (left and right) of vitellaria has an efferent duct that fuses with the other efferent duct to form a small vitelline reservoir. The vitelline ducts are lined with ciliated epithelium.
The two basic types of female reproductive systems are illustrated in Figure 19.9. The two types are distinguished by the connections of the vagina and the presence or absence of a genitointestinal canal. The vagina may be present or absent and may be doubled when present. Vaginal openings may be dorsal, ventral, or lateral. In species possessing a "true" vagina, its duct leads directly to the oviduct. The second type of reproductive system has a "ductus vaginalis" connecting the vitelline canals to the vagina. The function of the genitointestinal canal is unclear. Perhaps it represents a vestigial duct by which eggs were passed into the gut to be expelled through the mouth.
In species with a penis too large for entry into the vagina, a spermatophore is placed near the vaginal opening and the sperm make their way into the vagina and further into the female system. One species practices a type of "hypodermic injection" of sperm. Diclidophora merlangi uses its suckerlike penis to grasp a papilla of tegument and then sperm enter after spines on the penis breach the tegument. Fertilization occurs in the oviduct or ovary itself. The zygote and associated vitelline cells make their way to the ootype. There is a Mehlis' gland around the ootype, but its function is unclear. The ootype seems to determine the shape of the egg. Many species' eggs have one or more filaments that apparently serve to attach the egg to a host or to a substrate.
Although eggs are produced rapidly, they pass out of the worm rapidly, too. Hence, few eggs are present in a given worm at any one time. In most species, the eggs pass from the ootype into a uterus and then to an opening in the genital atrium. The ejaculatory duct is also located in the genital atrium.
Male Reproductive System
Although usually round or oval, testes may be lobated. One testis is found in most species, but up to 200 testes occur in at least one species. The vas efferens extends from the testis and expands or fuses with the ejaculatory duct. Unlike cestodes and trematodes there is no cirrus pouch or eversible cirrus. Ejaculatory duct structure varies among species. In some, it is simple, terminating within a shallow suckerlike genital atrium, which propels sperm into the female system. In other species, the tissues surrounding the terminal ejaculatory duct are thick and muscular forming a papillalike penis. Many species have a sclerotized distal ejaculatory duct. Some species have a saclike seminal vesicle and most species have unicellular prostatic glands. More complex structures are found in some species in which a sclerotized copulatory apparatus joins with the ejaculatory duct. The apparatus consists of a penis and an accessory piece. These structures are consistent within a species and can help with species identification. The structures are found in a sac and are controlled by muscles.
Development
Little is know about the life cycles of most monogeneans, although most seem to have a single host life cycle with an egg, oncomiracidium, and adult.
Oncomiracidium
Figures 19.10 and 19.11 illustrate the oncomiracidium that hatches from the egg and resembles a ciliated protozoan. It is elongate with three zones of cilia; one in the middle and one at each end. A nonnucleate, interciliary syncytium separates the zoned of cilia. The oncomiracidium has cephalic glands with efferent ducts opening on the anterior margin and they often have eyes. Well-differentiated excretory pores and digestive tract are found in the oncomiracidium. The larvae swim until they contact a suitable host. They then attach, lose their cilia, and develop into adults. The rates for development into adults are unknown.
The worm's egg production is timed to coincide with the breeding period of the fish so that transmission of the larva to a suitable host is enhanced. Several adaptation exist in life cycle that assist transmission to the host. Representative life cycle will be studied in the laboratory and your textbook presents some fascinating, even bizarre, examples.
Phylogeny
Current thought among systematists, is the the monogeneans are most closely
related to the cestodes.
Eucestoda (True Tapeworms)
Introduction
Sexually mature tapeworms live in the intestine of all classes of vertebrates. Two species are known from invertebrates: Archigetes spp. from the coelom of a freshwater oligochaete and Cyathocephalus truncatus from the hemocoel of an amphipod. Most cestodes have complex life cycles with more than one host and they have been of interest to humans since ancient times.
Morphology
Strobila
The strobila (Figure 20.3) is a linear series of both sets of sex organs (genitalium) surrounded by a proglottid or proglottis. Most cestodes have multiple proglottids or are polyzoic. The order Caryophyllidea contains species with only one genitalium are called monozoic (Figure 21.11). Some polyzoic species have only a few proglottids, while others have thousands. Constrictions exist between proglottids giving the appearance of segmentation. However, the tegument and muscles are continuous between segments leading some researchers to contend that the term segment should not be used. Some species lack any kind of constriction between segments to further confuse the issue. Therefore, do not use segment and proglottid as synonyms and do not confuse "segments" of tapeworms with the segments found in the truly metameric annelids and arthropods.
In most polyzoic species, new proglottids are produced near the anterior end in a process called strobilation. Each proglottid moves toward the posterior as the new one takes its place. As the proglottids progress to the posterior, they become sexually mature. The proglottids at the posterior end of the strobila will have copulated and produced eggs. Proglottids can copulate with themselves, other proglottids in the strobila, or proglottids from other worms, depending on the species. Proglottids with fully developed eggs or shelled embryos are termed gravid. If the posterior margin of a proglottid overlaps the anterior end of the next proglottid, the strobila is said to be craspedote; if not, it is acraspedote (Figure 20.4).
Proglottids often detach when they reach the end of the strobila. In some species the proglottids pass out intact with the host feces, while in others, the proglottid disintegrates and releases the eggs, which pass out in the feces. The release of proglottids is called apolysis. In some species the eggs are released and then the proglottid detaches (pseudapolysis or anapolysis). In other species, the segments shed while immature and lead an independent existence in the gut while maturing (hyperapolysis).
Scolex
Most, but not all, cestodes have an anterior scolex (scolices, plural) that bears one or more of a variety of structure that help anchor the tapeworm in the host gut (Figure 20.5). The anchoring structures are suckers, grooves, hooks, spines, glands, tentacles, or combinations of these (Figure 20.6). In some species the scolex is simple or even absent. A pseudoscolex is present in other species that have lost the scolex; it is a modification of the anterior end of the strobila to function as a holdfast (Figure 20.7).
Three types of suckerlike organs are found on scolices: bothridia, bothria, and acetabula. Bothridia are usually grouped in fours, are muscular, project sharply from the scolex, and can have highly, mobile leaflike margins. Bothria are usually two in number, but as many as six are found in some species. They are shallow pits or longer grooves that are arranged in lateral or dorsoventral pairs. An acetabulum is more or less cup shaped, circular, or oval in outline, with a heavy muscular wall. Usually four, equally spaced acetabula are found on a scolex. Many species have accessory suckers and/or a variety of proteinaceous hooks to help anchor the scolex. Worms with acetabula have hooks arranged in one or more circles anterior to the suckers, borne on a protrusible, dome-shaped area on the apex of the scolex called the rostellum. Presence, absence, shape, and arrangement of hooks are taxonomically important.
A variety of gland cells have been found on scolices, but their functions remain unclear. It is thought that the secretions may aid adhesion of the scolex, at least in some species. Some species have apical organs (Figure 20.8) that may help regulate development of the worm (Hymenolepis diminuta) or secrete proteolytic substances that aid penetration.
The primary neural ganglion of the worm is found in the scolex. It has numerous sensory endings on the anterior surface that can probably detect both chemical and physical stimuli. These may help place the scolex in a suitable location within the host gut.
The neck is a relatively undifferentiated portion of the worm between the scolex and the strobila. It contains the stem cells that give rise to the proglottids.
Tegument
Cestodes have no digestive tract and must absorb all of their nutrients through the tegument. Hence, this is one of the most studied body parts of tapeworms. As with other flatworms, it is a living, metabolically active tissue.
The general structure of the tegument is similar in all cestodes studied, with some variations among species. Its basic structure is similar to that seen for the trematodes. One major difference is the covering of minute microvilli called microtriches (microthrix, singular) found on the cestode tegument (Figure 20.9). These completely cover the surface of the worm, even the suckers. The microtriches serve to increase the absorptive surface area of the tegument. Associated with the plasma membranes of the microvilli is a layer of carbohydrate-containing macromolecules called the glycocalyx. The glycocalyx contains molecules that seem to mediate a number of host-parasite interactions. These interactions include: enhancement of host amylase activity; inhibition of host trypsin, chymotrypsin, and pancreatic lipase activity; absorption of cations; and adsorption of bile salts. These phenomena may enhance nutrient absorption, protect the worm from digestion by the host enzymes, and maintain the integrity of the worms surface.
Calcareous Corpuscles
These structures are found in most cestodes and a few trematodes. The corpuscles are 12 to 32 um in diameter and are produced by calcareous corpuscle cells that are destroyed in the process. They are made up of calcium and magnesium carbonates as well as a hydrated form of calcium phosphate embedded in an organic matrix. The organic matrix is arranged in concentric rings with a double outer envelope and it contains protein, lipid glycogen, mucopolysaccharides, alkaline phosphatase, RNA, and DNA. Their function is unknown. One suggestion is that they are part of a buffer system that protects the worm against the organic acids produced during metabolism. A second suggestion is that they provide storage areas for carbon dioxide or ions that can be used when these substances are in short supply. A third idea is that they are excretory products.
Muscular System
The muscular fiber (cell) structure of Hymenolepis diminuta is the best studied cestode system and the cytological details are probably similar for most cestodes and even trematodes. The muscle cells have a contractile myofibril and a noncontractile myocyton. The myofibrils contain actin and myosin and the muscle cells are nonstriated and lack the transverse sarcolemmal tubules (T tubules) found in striated muscle. As with smooth muscle in vertebrates that also lacks striation and T tubules, contraction of cestode fibers is slow. The myocytons make up the bulk of the parenchyma of the cestode, which has led to them be called parenchymal cells. The myocytons contain a nucleus, rough endoplasmic reticulum, free ribosomes, a Golgi complex, few mitochondria, abundant glycogen, and stored lipids.
The contractile portions of the muscle cells are arranged in bundles in specific regions of the worms. Just internal to the distal cytoplasm are bundles of longitudinal and circular fibers. More powerful muscles lie just beneath these superficial muscles. Dorsoventral, transverse, and even radial muscle fibers may also be present in the worm. The arrangement of muscle bundles varies with species and can even serve as taxonomic characters.
Not surprisingly, the internal musculature of the scolex is complex and allows a great deal of mobility. In the Trypanorhyncha, three muscle types have been identified. Peripheral myofibers are similar to the previously described muscle cells, tentacle retractor muscles, and tentacle bulb muscles. The tentacle bulb muscles have many motor end plates suggesting a high degree of nervous system control.
Nervous System
The scolex contains the primary nerve center for the tapeworm. The nerve centers consists of a complex of ganglia, commissures, and motor and sensory innervation. The simpler the holdfast structures associated with the scolex, the less complex the nerve center and vice versa. Figure 20.13 illustrates a more complex nerve center from a species with complex holdfast structures. The scolex may also have sensory endings and stretch receptors.
Longitudinal nerves extend posteriorly from the anterior ganglia and as they proceed they are connected by intraproglottidal commissures in a ladderlike arrangement. Small nerves arise from the longitudinal nerves to supply the body muscles and sensory endings. The vagina and cirrus are well-supplied with nerves and the genital pore has more sensory endings than other parts of the strobila.
Histochemical and immunocytological studies indicate that serotonin is an important excitatory neurotransmitter and acetylcholine is the main inhibitory neurotransmitter. At least 20 different neuropeptides have been found, but their functions are still unclear.
Sensory endings seem to include tactoreceptors and chemoreceptors. One type of common sensory ending has a modified cilium projecting as a terminal process (figure 20.14). This type of structure was also seen in the other groups of flatworms.
Excretion and Osmoregulation
The cestodes have the protonephridial flame bulb system typical of the flatworms. They function in the same manner as described previously for the digeneans. Figure 20.16 illustrates a flame cell protonephridium and these are embedded throughout the parenchyma. The ductules of flame cells appear to be syncytial as opposed to being formed by a single cell as is the case for the trematodes. The excretory ducts are lined with microvilli (Figure 20.17) suggesting they are involved in transport, such as active transport of excretory wastes and they may also help to regulate ionic concentrations of the excretory fluid. When sampled, the excretory fluid has been found to contain glucose, soluble proteins, urea, ammonia, and lactic acid.
The collecting ducts join the main excretory canals that run the length of the strobila. Usually a cestode will have ventrolateral and dorsolateral pairs of excretory canals (Figure 20.15). The dorsal pair tends to have a smaller diameter. The ventrolateral canals are often connected at the posterior margin of the proglottid by a transverse canal. In the scolex, the dorsal and ventral canals unite. Posteriorly, the two pairs of canals merge into an excretory bladder with a single pore to the outside. When the terminal proglottid detaches in polyzoic species, the canals empty independently to the outside at the end of the strobila. In some species, the major canals may empty through short, lateral ducts. Some species lack dorsal and ventral ducts and have a network of canals, instead.
End products of cestode metabolism , such as short-chain organic acids, are probably excreted through the tegument, not the excretory system. The tegument is also important in osmoregulation in cestodes.
Reproductive Systems
The vast majority of tapeworms are hermaphroditic. A few species from water birds and two from a stingray are dioecious. Each proglottid normally has one complete set of female and male sex organs, but some species have two sets of genitalia per proglottid (Figure 20.4b), and a few species have one male and two female systems in each proglottid.
As the proglottid moves toward the posterior, the reproductive systems mature, sperm are transferred, and oocytes are fertilized. The male organs tend to mature first and produce sperm that are stored until needed; this is called protandry or androgyny. In a few species the ovary matures first; this is called protogyny or gynandry. There are many variations in arrangement, structure, and distribution of sex organs in tapeworms.
Female Reproductive System
The female reproductive system is illustrated in Figures 20.18 & 20.19. Many of the structures are the same as those seen in the digeneans. The ovary and its accessory structures are variable in size, shape, and structure according to species and are collectively termed the oogenotop. The vitelline cells may be scattered as follicles in various patterns, or they may be arranged as a compact vitellarium. As in the trematodes, the eggs are ectolecithal. Maturing oocytes leave the ovary via a single oviduct, which has a controlling sphincter, the oocapt.
Oocytes are arrested in meiosis I and sperm penetration is necessary to stimulate resumption and completion of meiosis. Sperm penetration occurs in the proximal oviduct. One or more vitelline cells enter the oviduct and join the zygote. Together they pass to the ootype. Unicellular Mehlis' glands surround the ootype and appear to secrete a thin membrane around the zygote and vitelline cells. Shell formation is completed by the vitelline cells and, often, the embryo cells. In the Pseudophyllidea, the egg is covered by a thick capsule of sclerotin (Figure 20.20). In many species, the shelled embryo passes from the host where a free-swimming larval stage emerges after a period of development. This larval stage is then eaten by an intermediate host.
In Figure 20.20 we see three other variations in shell formation in the cestodes, based on contributions from the embryo. In the Dipylidium type, there is a thin capsule and an embryophore. The Taenia type has a very thin capsule and a thick embryophore. The Stilesia type is formed by species with no distinct vitellaria and the cellular covering is apparently laid down by the uterine wall.
As the zygote and vitelline cells pass through the ootype, Mehlis' gland secretions are added that may cause exocytosis of shell materials from the vitelline cells and form the structural support component for the capsule. The developing embryo leaves the ootype and passes into uterus where embryonation is completed.
The uterus structure varies significantly with species. It may be lobulated, circular, or reticulated. It can be a simple sac, a simple tube, or a convoluted tube. In some species the uterus disappears and the eggs are enclosed within the hyaline egg capsules embedded within the parenchyma. In some species, one or more fibromuscular structures called parauterine organs form, attached to the uterus. The eggs then pass from the uterus into the parauterine organ, which assumes the uterine function. The uterus will then disintegrate.
Male Reproductive System
Figures 20.18 & 20.19 illustrated the male reproductive system. There may be one or many testes, each of which has its own vas efferens. These unite to form the vas deferens that will take the sperm toward the genital pore. The vas deferens may be a simple duct or may have convolutions or an external seminal vesicle for sperm storage. The vas deferens makes its way to the muscular cirrus pouch, which contains the final organs in the male system. The last part of the vas deferens may form a convoluted ejaculatory duct or an internal seminal vesicle. The muscular cirrus serves as the male sex organ and it may or may not have spines. It can evaginate through the cirrus pore and invaginate into the cirrus pouch.
The reproductive organs of both sexes usually empty into the genital atrium.
The atrium may be a simple, sunken chamber or it may be equipped with spines,
stylets, glands, or accessory pockets. The cirrus pore may open on
the margin or on the flat surface of the proglottid. If two male systems
are present, they open on opposite margins of the proglottid.
Development
Introduction
Almost all cestode life cycles involve two hosts. One exception is the mouse and human tapeworm Vampirolepis nana. Previously this worm was placed in the genus Hymenolepis, but it has features, such as an armed rostellum, that justify a separate genus. Surprisingly, relatively few complete life cycles have been determined for tapeworms. There are entire orders of tapeworms for which not one complete life cycle has been determined. Of the known life cycles, a great deal of variety exists.
Most sexually mature tapeworms live in the intestine or its diverticula and rarely in the coelom of a vertebrate host. The two tapeworms that mature in invertebrates were mentioned earlier. Tapeworms can live from a few days to many years depending on species. Mature worms may produce a few eggs to millions of eggs during their life spans. Mortality is high, especially for those that produce millions of eggs.
As mentioned earlier, most tapeworms are hermaphroditic and can self-fertilize. Some species lack a vagina for sperm reception from the cirrus. In some of these species hypodermic impregnation is utilized (similar to what occurs in some species of monogeneans). In these species, the cirrus is forced through the body wall, and sperm are deposited within the parenchyma (Figure 20.22). How they reach the seminal receptacle is unknown.
In the few species that are dioecious, it is unclear what determines the sex of a given strobila since they appear to have the potential to be either female or male. It is clear that at least two worms must be present for sex determination to occur because when only one worm is present, it is usually female, in the genus Shipleya. When two worms are present, one is usually a male.
Vertebrates and invertebrates can serve as intermediate hosts for tapeworms. Almost every group of invertebrate examined has been found to harbor juvenile tapeworms. The most common invertebrate hosts are crustaceans, insects, mites, annelids, and mollusks. Generally, when a tapeworm occurs in an aquatic definitive host, its larval forms are found in aquatic intermediate hosts. The same usually holds for terrestrial hosts. Vertebrate intermediate and paratenic hosts are found among fishes, amphibians, reptiles, and mammals. The tapeworms in paratenic hosts usually mature in vertebrate hosts that prey upon the paratenic host(s).
Larval and Juvenile Development
Tremendous variation exists in larval forms in the known life cycles. However, the following stages occur in almost all developmental sequences: (1) embryogenesis occurs within the egg giving rise to a larva or oncosphere; (2) the oncosphere hatches before or after being eaten by the next host, where it penetrates to a parenteral site; (3) the larva metamorphoses in the parenteral site to a juvenile (metacestode) usually with a scolex; and (4) the adult develops from the metacestode in the intestine of the same or another host. The oncosphere of all Eucestoda have three pairs of hooks (Figure 20.23) and are called hexacanths. Oncospheres of the Pseudophyllidea and a few Tetraphyllidea are free-swimming, after hatching, have a ciliated inner envelope, and are called coracidia (Figure 20.24). Oncospheres of the gyrocotylideans and amphilinideans have 10 hooks (decacanths), are also ciliated and are called lycophoras.
In species with a coracidium, it must be eaten by an intermediate host within a short time before its energy stores are used up. Once ingested, usually by an arthropod, the coracidium will shed its ciliated inner envelope and actively use its six hooks to penetrate the gut of its host. In the hemocoel it metamorphoses into a procercoid (Figure 20.25). The hooks end up in the posterior end of the procercoid in a structure called the cercomer. The procercoid is a stage in which the larval hooks are still present, but the definitive holdfast organ has not developed. When the scolex develops, the larval stage is called the plerocercoid (Figure 20.25), and the strobila may begin to form in this stage, with or without proglottid formation.
In some pseudophyllidean species, the plerocercoid develops to the point that little further development will occur when the worm enters its definitive host. In these worms, the gonads may mature within 72 hours and start producing eggs 36 hours after maturation. In the Proteocephalata, there is no procercoid and a first-stage plerocercoid develops within the arthropod intermediate host and a second-stage plerocercoid will develop in the parenteral site of a second intermediate host. To complicate matters further, in some proteocephalatans, the metacestode development (second-stage) may go to completion in the gut of the definitive host, or the metacestodes may develop through several sites; parenterally in an intermediate host, then parenterally in the definitive host, and finally enterally in the definitive host. These various larval forms that must migrate through host tissues have a number of penetration glands to aid penetration and movement through the tissue.
The cyclophyllideans lack procercoids and plerocercoids in their life cycles. The larvae are fully developed and infective when they pass from the definitive host. The oncosphere penetrates the gut of the intermediate host to enter the parenteral site. Metamorphosis to a cysticercoid or a cysticercus type of metacestode occurs at this site. Cysticercoids (Figures 20.25 & 20.26) are solid-bodied larvae with a fully developed scolex embedded in the body. It is surrounded by cystic layers, and the cercomer is outside the cyst. In the gut of the definitive host, the cercomer will be digested away, along with parts of the cyst. For a few species, cysticercoids have been found that undergo asexual reproduction by budding.
In the cyclophyllidean family Taeniidae, the metacestode is a cysticercus (Figures 20.25, 21.12, & 21.17). Cysticerci have a scolex that is both invaginated and introverted. The scolex forms on a germinative membrane enclosing a fluid-filled bladder. Variations on this theme are seen in which asexual budding occurs producing cysticerci that are often of medical and veterinary importance (see below).
Below are several other types of metacestodes that are mainly modifications
of the previously mentioned larval forms.
Relatively few species have been studied well and generalizations from these to all tapeworms is not recommended. However, for those species that have been studied, a great deal of information is available.
In the gut of the definitive host, certain stimuli will cause the juvenile tapeworm to excyst, evaginate, or both and begin growth and development to the sexually mature adult. Host enzymes and bile salts are frequently necessary to stimulate excystment.
In the pseudophyllidean genera Ligula and Schistocephalus, an increase in temperature to that of the definitive host is necessary for maturation of the plerocercoid. This temperature activation is accompanied by a tremendous increase in the rate of carbohydrate catabolism, excretion of organic acids, and levels of Krebs' cycle intermediates. In Diphyllobothrium dendriticum, a burst of neurosecretory activity occurs during activation of the plerocercoids. In Echinococcus, the rostellum must contact a suitable protein substrate for strobilar growth to occur.
Size of the infecting juvenile, size and diet of the host, species of the worm and the host, presence of other worms, and the immune and/or inflammatory state of the host intestine will all influence strobilar development. When conditions are optimal, many tapeworms can grow at tremendous rates. For example, Hymenolepis diminuta can increase its weight 1.8 million times in 15 to 16 days. This growth rate as well as ease of use in the laboratory have made H. diminuta a favorite study organism for parasitologists.
The primary nutrient that tapeworms absorb across their tegument is glucose. This must be supplied in the host diet as a polysaccharide that is broken down to glucose for the worm to be able to absorb it. If the glucose is supplied directly or as a breakdown product of sucrose, the host gut is able to outcompete the worm in absorption of the glucose. The worm's growth will be slowed, in this case.
The crowding effect is an important phenomenon that can influence tapeworm growth. It occurs when other tapeworms or other gut parasites are present in the host. In the crowding effect, the parasite biomass adjusts according to the carrying capacity of the host. On average, the weight of individual worms is inversely proportional to the number of worms present. Hence, the total worm biomass and the number of eggs produced is the same and is maximal for that host, regardless of the number of worms present. The mechanisms by which the crowding effect might work are not well known.
As adult worms reach their maximum size, the growth rate will decrease and production of new proglottids will only replace those that are lost by apolysis. Some tapeworm species die after a period of time and pass out of the host, while other species seem to be able to live as long as their hosts. Taeniarhynchus saginatus may live as long as 30 years in humans. Hymenolepis diminuta has been kept alive in the laboratory for as long as 14 years by Read who would remove the worm, sever the strobila in the germinative area and surgically reimplant the worm in another rat.
Some tapeworms are fairly mobile within the host's gut. They may move as they grow or even move down and then back up the gut. Hymenolepis diminuta undergoes a diurnal migration in the rat's gut (Figure 20.29). The migration correlates with the rat's feeding behavior and can be modified by modifying the time the rats are fed.
Metabolism
Nutrient Acquisition
Nutrients are absorbed across the tegument by active transport, facilitated diffusion, and simple diffusion. Some plerocercoids and cysticerci are capable of pinocytosis, but is it not clear if adult tapeworms have this ability. Glucose is the main carbohydrate molecule that can be absorbed and some galactose can be absorbed. Others monosaccharides may be absorbed, but only glucose and galactose can be metabolized. As in many other animals, glucose absorption is coupled to a sodium pump mechanism that allows it absorption against a concentration gradient. The glucose can be stored as glycogen.
Amino acids are absorbed, but their metabolism is poorly understood. Purines and pyrimidines are absorbed by facilitated diffusion. The mechanism of lipid absorption is not understood, but may involve diffusion. Vitamin requirements have been established in two tapeworms. H. diminuta requires an external supply of the vitamin pyridoxine. It is inferred that Diphyllobothrium latum has a requirement for vitamin B12 because the worm accumulates large amounts of it. The worm can compete successfully with the host and may even cause pernicious anemia in the host.
Energy Metabolism
Tapeworm metabolism is similar to that of the trematodes. They are facultative anaerobes that derive most of their energy from glycolysis. They do not use lipids for energy storage and depend on glycogen stores. During periods of host starvation, glycogen stores can be depleted rapidly by H. diminuta. Within 48 hours, 80% of the worm's glycogen stores can be used up. When nutrients are again available, the glycogen stores are built up rapidly.
Additional ATP can be produced by utilizing malate formed from the fixation of carbon dioxide. THe malate enters the mitochondria and goes through a series of reactions that produces two more ATPs (Figure 20.30).
Certain metacestodes appear to have active Krebs cycle mechanisms. However, adults cestodes do not seem to utilize this metabolic pathway.
Some cestodes have a classical electron transport chain, but it appear to be of little importance to the adult worms. A different type of electron transport system called the o-type (Figure 20.31) appears to be of greater importance in these facultative anaerobes. In this branched system, the electrons are transported to fumarate and oxygen depending on whether conditions are anaerobic or aerobic.
Lipid and amino acid metabolism and use in cestodes are poorly understood, aside from the obvious use of amino acids in enzymes, structural proteins, and so on.
Nitrogenous end products excreted by H. diminuta include urea, ammonia, and alpha amino nitrogen.
The ability to absorb purines and pyrimidines underlines the fact that tapeworms can synthesize their own nucleic acids.
Effects on Hosts of Tapeworm Metabolites
Tapeworm metabolites produced by some species have hormone-like effects on their hosts. Ligula plerocercoids prevent their fish hosts from reproducing by preventing gonad development and suppression of gonadotropin-producing cells in their pituitary glands. However, no metabolite has been identified and the mechanism of this suppression is not understood.
A substance has been identified that is produced by plerocercoids of Diphyllobothrium mansonoides referred to as plerocercoid growth factor (PGF). It closely resembles human growth factor (hGF) and acts like a growth hormone in rats (Figure 20.32). PGF has the same binding specificity as hGF and monoclonal antibodies raised against hGF cross react with PGF. How can this be? One hypothesis is that the gene for PGF is a human gene (for hGF) that has been sequestered by the tapeworm during its evolution. Some evidence suggests that PGF may also be able to suppress the immune system; a definite advantage for the worm.
Phylogeny
The phylogeny of the cestodes is undergoing tremendous revision. One could say that heated arguments are even occurring. However, as previously stated, the monogeneans and cestodes appear to be more closely related to each other than to the digeneans. Figure 20.33 is a cladogram of hypothetical relationships among groups within the infraclass Cestodaria.