We will follow the classification scheme utilized by Roberts and Janovy. The classification of acanthocephala is difficult because they share so few features with other groups. They have been variously associated with nematodes and rotifers over time and recent work suggests that rotifers are their closest relatives. When you encounter terms which are unfamiliar refer to your glossary for the definitions.
Acanthocephala were first recognized in the 17th century, but it was not until the 20th century that they were acknowledged to be a separate phylum. They are rarely found in humans and domestic animals, so that most clinicians are unfamiliar with the group. The exception to this is Macracanthorhynchus hirudinaceus, which is a cosmopolitan parasite of swine. All members of the phylum are parasitic. The life cycle usually involves a vertebrate definitive host and arthropod intermediate host.
Acanthocephala are little more than bags of gonads. In both sexes, the nervous system, muscular system, excretory system, and circulatory system are reduced. The digestive tract is completely missing. The worms are pseudocoelomate with a holdfast proboscis at the anterior end. Figure 31.1 illustrates the general body structure of an acanthocephalan. Prominent features are the proboscis, neck, and trunk. The hollow, fluid-filled proboscis is covered with hooks and its shape varies among species from cylindrical to spherical (Figure 31.2). The size, shape, and number of hooks are important taxonomic characters. Proboscis retractor muscles are attached to the inner apex of the proboscis and extend the length of the proboscis and neck before inserting into a muscular sac known as the proboscis receptacle (Figures 31.1 and 31.3). Contraction of the proboscis retractor muscles invaginates the proboscis and the hooks are then completely inside. Evagination of the proboscis is effected by contraction of the proboscis receptacle, which forces the proboscis out by a hydraulic system. The cerebral ganglion or brain is located within the proboscis receptacle.
Presoma is the collective name for the proboscis and its receptacle. The neck is smooth, unspined and between the posterior end of the proboscis and the trunk. Some species possess neck retractor muscles that work with the proboscis retractor muscles to withdraw the entire anterior end into the trunk. A sensory pit is found on each side of the neck in some species, while many species have a pair of similar pits on the proboscis tip.
Metasoma is another name for the trunk. It is covered by a tegument (as are the proboscis and neck) and it has muscular internal layers. Some species have spines embedded in the tegument that appear to help maintain close contact with the host's intestinal mucosa. The reproductive system is found in the trunk. The trunk absorbs host nutrients and helps distribute them within the worm. Living worms have a wrinkled, bilaterally flattened trunk that will become turgid when put into a hypotonic solution. This phenomenon is utilized when preparing the worms for study because it usually forces the proboscis to evaginate, which is important in identifying the species.
The body wall is syncytial with numerous nuclei and a complex series of internal, interconnected canals called the lacunar system (Figures 31.4, 31.5, and 31.6). The nuclei are large and few in number in some species, while in others they fragment during development and are widely distributed in the body wall. Species with few nuclei exhibit eutely, or nuclear constancy. This, too, can serve as a taxonomic character.
There are several distinct layers to the tegument (Figure 31.4). From the outside in, they are:
The striped zone is 4-6 um thick and is perforated by crypts that are 2-4 um deep and open to the surface by pores. The crypts give the zone a striped appearance under the light microscope, hence the name. The crypts greatly increase the surface area. The necks of the crypts have a filamentous molecular sieve through which particles less than 8.5 nm can pass. These particles can undergo pinocytosis by the crypt membrane, although the importance of pinocytosis in nutrient acquisition is still not fully understood. Numerous lipid droplets, mitochondria, Golgi complexes, and lysosomes are found in deeper regions of the zone.
The felt-fiber zone is next and contains mitochondria, numerous glycogen particles, vesicles, and occasionally lysosomes and lipid droplets. Just inside the felt-fiber zone is the radial fiber zone that constitutes about 80% of the thickness of the body wall. Within the radial fiber zone are large bundles of filaments that pass radially through the cytoplasm, nuclei of the body wall, and large lipid droplets. Glycogen particles, Golgi complexes, lysosomes, and mitochondria are also found in this zone. The perinuclear cytoplasm contains rough endoplasmic reticulum. The lacunar canals pass through the radial fiber zone.
The proboscis wall is similar in structure to the body wall, but has fewer crypts, a thinner radial zone, and no felt-fiber zone.
Lacunar System and Muscles
The function of the lacunar system has been unclear, but research done by my friends Dr. Tommy Dunagan and the late Dr. Donald Miller has helped to elucidate the function and the association of the system with the circular muscle layer.
There are two unconnected parts to the lacunar system, (1) the presomal system in the proboscis and neck, and (2) the metasomal system associated with the body wall. Channels in the presomal system run into a pair of lemnisci, which are extensions of the radial fiber zone growing from the base of the neck into the pseudocoelom. The central canal of each lemniscus is continuous with the presomal lacunar system. The lemniscal function is unknown, but it has been suggested that they contribute to the hydraulics of the proboscis mechanism.
The metasomal lacunar system is a complex network of interconnected canals. The arrangement and location of the lacuni are species-specific and serve as useful taxonomic characters. Most species have a pair of main longitudinal canals either lateral or dorsal and ventral in arrangement. The main canals are connected by a series of transverse canals (Figure 31.5). Some species have a pair of medial longitudinal canals connected to the to the other dorsal and ventral canals by short radial canals attached to circular ring canals (Figure 31.5). The medial canals are on the pseudocoel side of the body wall and the radial canals pass through the muscles to connect to the ring canals.
The body-wall muscles include an inner longitudinal layer surrounded by an outer circular layer (Figure 31.6). The muscles have an unusual hollow structure with numerous interconnecting anastomoses. The lumina of the muscles are continuous with the lacunar system suggesting that the circulation of lacunar fluid might serve to bring nutrients to and remove wastes from the muscles. Contraction of the longitudinal muscles would force fluid into the circular muscles and vice versa. Hence, the current thought is that the lacunar system serves as a fluid transport system combined with a hydrostatic skeleton.
Acanthocephalan muscles are unlike muscles in other organisms because they have low membrane potentials, are electrically inexcitable, and exhibit slow conduction. Depolarization of the muscles is spontaneous and rhythmic. Acetylcholine appears to stimulate the muscles, but nervous control of contraction has not been well demonstrated. If nervous system control does occur it is thought to do so via the rete system, which is a highly branched, anastomosing network of thin-walled tubules that lie on the medial surface of the longitudinal muscles or between the longitudinal and circular layers. The rete system may be modified muscle cells.
The nervous system is reduced and very simple in the acanthocephala. The cerebral ganglion lies in the proboscis receptacle and has relatively few nerves issuing from it. The anterior proboscis nerve and the lateral posterior nerves are the largest nerves branching from the ganglion. The nerves supply the two lateral sense organs and apical sense organ, if present. A large, multinucleated support cell is located ventrally and slightly anterior to the cerebral ganglion. Processes lead from this cell to the sense organs, but they are not nerves and their function is unknown. They may have a secretory function that can help explain the host's inflammatory response to the worm's proboscis.
Most acanthocephala utilize diffusion across the body wall to effect excretion. However, members of the Family Oligoacanthorhynchida possess two protonephridial excretory organs. These organs have numerous anucleate flame bulbs with tufts of flagella that may or may not be encapsulated. In females these organs are attached to the uterine bell (see below) and empty into the uterus; in males they are attached to the vas deferens and empty through it.
Osmoregulatory capabilities are limited in the Acanthocephala. In a hypotonic solution they swell and in hypertonic solutions they become flaccid. The pseudocoelomic fluid osmotic pressure is close to or slightly above that of the intestinal contents of the host.
Acanthocephalans have separate sexes and females are usually larger than males (Figure 31.3). Ligament sacs are attached to the posterior end of the proboscis and extend to near the distal genital pores of both sexes. Gonads and accessory organs are contained within these sacs. In some species the ligament sacs are permanent; in others they break down as the worm matures.
Acanthocephalans have a very unique ovary that fragments into ovarian balls, often prior to maturation. The ovarian balls consist of oogonia floating freely in the ligament sac. The balls increase slightly in size prior to insemination. A muscular uterine bell is attached to the posterior end of the ligament sac (Figure 31.8). This organs sorts the mature eggs from the immature eggs, allowing the mature ones to pass into the uterus and vagina and out the genital pore. The immature eggs are returned to the ligament sac.
Following copulation, the spermatozoa migrate from the vagina, through the uterus and uterine bell into the ligament sac. The oocytes in the ovarian balls are fertilized and after the first few cleavages break away from the ovarian balls exposing the underlying oocytes. Fertilization is staggered as the outermost oocytes are fertilized first and several stages of early embryogenesis can be found in a single female. The developing embryos float freely in the pseudocoelomic fluid undergoing further development as shelled embryos. Fully developed embryos are called shelled acanthors.
The shelled acanthors are pushed into the uterine bell by peristaltic action and may follow one of two routes. If they are not fully developed they will pass through slits in the bell and return to the pseudocoelom. Mature embryos are too large to pass through the slits and will continue on through the uterus, vagina and eventually out the genital pore into the host's intestine. This mechanism is quite efficient and research suggests that no immature embryos are released into the uterus.
In most species two testes occur in the males and location and size are fairly consistent (Figure 31.3). Mature spermatozoa pass from each testis into a vas efferens that leads to a common vas deferens or penis. The spermatozoa are headless, slender threads. Several accessory organs are present in the male system including the cement glands, which are syncytial organs with one or more giant nuclei or several nuclear fragments. When more than one gland is present they are joined by slender connections. The cement glands secrete a tanned protein called copulatory cement, which in some species is stored in a cement reservoir. The cement is secreted after copulation and forms a copulatory cap or cement plug that blocks the vagina, preventing fertilization by other males. The cap will eventually disintegrate, so that fully developed shelled acanthors can be released.
The copulatory bursa (Figure 31.7) is a specialized, bell-shaped
extension of the body wall that remains invaginated in the posterior end of
the body except during copulation. The Saefftigen's pouch is
a muscular sac attached to the base of the bursa that contracts and forces
fluid into the bursa to evert it by hydrostatic pressure. Sensory papillae
line the bursa and when it contacts a female, it clasps her by muscular contraction,
and sperm transfer occurs via the penis.
Acquisition of Nutrients
The nutrient uptake and metabolism of only one species (Moniliformis moniliformis) has been well studied, although some work has been done on other species. Therefore, generalizations about the applicability of the study results is problematic. Most of the information below is based on the few species that have been studied.
All nutrient molecules must be taken up through the body wall, just as in the Cestoda.
Triglycerides are absorbed by the presoma and eventually accumulate in the lemnisci. Amino acids are absorbed, in part, by stereospecific membrane transport systems. The surface of M. moniliformis contains peptidases that can cleave several dipeptides to allow absorption of the resulting amino acids by the worm. In some species lysine is absorbed across the metasomal tegument and accumulates in the nuclei and the outer muscle belt. Thymidine is absorbed and incorporated into the DNA in the perilacunar regions and into the nuclei of the ovarian balls and testes. Radioactive thymidine is not found in the nuclei of the body wall and it is assumed that the DNA synthesized in the wall is mitochondrial.
M. moniliformis absorbs all of its carbohydrates from its host. The worm can absorb mannose, glucose, fructose, galactose, and several glucose analogs. The glucose locus serves as the site for absorption of glucose, while the other carbohydrates are absorbed at the so-called fructose site. Maltose and glucose-6-phosphate are hydrolyzed to glucose by enzymes before being absorbed. Unlike most glucose transport systems, the system in M. moniliformis is not coupled to sodium co-transport.
Acanthocephalan energy metabolism is adapted for facultative anaerobiosis. M. moniliformis can ferment the hexoses that are absorbed, but the Krebs cycle does not seem to be present the M. moniliformis or Macracanthorhynchus hirudinaceus. However, Echinorhynchus gadi does show evidence of the Krebs cycle. The end products of glycolysis in M. moniliformis are ethanol and lactate, rather than succinate.
Endogenous lipids are not metabolized during in vitro incubation of M. moniliformis suggesting that lipids are not used as a source of energy. The enzymes required for beta-oxidation of lipids show low activity levels or are absent completely.
Little is known about electron transport in acanthocephalans.
Development & Life Cycles (Figures 31.9, 31.10, 31.11)
Figure 31.9 illustrates a typical life cycle for an acanthocephalan. Arthropods serve as the intermediate host and the insect, crustacean, or myriapod must eat an "egg" (actually a shelled acanthor) that was released with the feces from the vertebrate definitive host. Once within the intermediate host, the parasite develops through several stages the last of which is infective to the definitive host. The definitive host consumes an infected intermediate host to continue the life cycle. A paratenic host is an unsuitable vertebrate definitive host in which the parasite will not mature, but will encyst in the peritoneal viscera. If the paratenic host is eaten by the proper definitive host, the life cycle will be completed. If not, it is a dead end for the parasite. A paratenic host can bridge the gap between microcrustacea and large piscivorous fishes. The small fish in Figure 31.9 serves as an example of a paratenic host.
We will examine the life cycle of Acanthocephalus dirus via live material at some point this semester.
Early cleavage is spiral and slightly distorted by the spindle shape of the eggshell. Between the 4-cell state and 34-cell stage, cell boundaries disappear and the entire embryo becomes syncytial. Nuclei migrate to the interior during gastrulation. The nuclei become smaller as they continue to divide and eventually they form a dense core of tiny nuclei called the inner mass. All of the internal organs of the worm develop from these nuclei. Depending on the species, the tegument develops from the uncondensed nuclei remaining in the peripheral area; or from a nucleus that separates from the inner mass, or from contributions from both.
The acanthor is fully embryonated and infective to the arthropod intermediate host. It is an elongated organism frequently possessing six or eight bladelike hooks at the anterior end. These hooks aid in penetration of the intermediate host's gut. In some species the hooks are replaced by small spines. Together the hooks or spines and their muscles are called the aclid organ or rostellum. Acanthors will not develop further until ingested by a suitable intermediate host. Acanthors can remain viable for months under normal environmental conditions. The acanthor will penetrate the host's gut to either completely enter the hemocoel or to lie just beneath the serosa. The acanthor will begin absorbing host nutrients and develop further into the next larval stage the acanthella. During the acanthella stage, the organ systems develop from the central nuclear mass and the hypodermal nuclei.
The final developmental stage is the cystacanth, which is infective
to the definitive host. No further development will occur until the
cystacanth is ingested by a suitable definitive host. The anterior and
posterior ends of the cystacanth are invaginated and the entire worm is encased
in a hyaline sheath. Only a small fraction of the large number of eggs
produced ever reach the cystacanth stage and few of these will be ingested
by a definitive host.
Effects of Acanthocephalans on their Hosts
One of the fascinating features of acanthocephala is their influence on the behavior, morphology, and other features of their intermediate hosts that tend to increase the probability of transmission to the definitive hosts. Cockroaches (Periplaneta americana and Blatella germanica) infected with M. moniliformis travel shorter distances, move more slowly, and spend more time on horizontal surfaces than do uninfected controls. Aquatic isopods (Caecidotea intermedius) infected with Acanthocephalus dirus are hyperactive, spend more time on top of leaf litter, and may be markedly lighter in pigmentation than are uninfected isopods.
Amphipods (Gammarus lacustris) infected with Polymorphus paradoxus change their phototactic response from negative to positive and the infected amphipods stay at the water's surface instead of diving in response to disturbance. They may even cling to floating vegetation. These behavioral modifications enhance the transmission of the worms to their definitive hosts (muskrats and surface-feeding ducks).
Acanthocephalans can cause severe damage to the intestines of their hosts. Complete perforation of the gut (Figure 31.12) can occur and this is often fatal. Secondary bacterial infection may lead to peritonitis, hemorrhage, pericarditis, myocarditis, arteritis, cholangiolitis, and other problems.
Although perforation may occur, there is usually little inflammatory response
to penetration of the proboscis although encapsulation may occur (Figure
31.13). At least one species (M. hirudinaceus) does produce
antigens that elicit an intense inflammatory response, but this species seems
to be the exception.
Classification of Acanthocephala (see pp. 480-481 in
Roberts & Janovy)