© 2002 by The Society for Integrative and Comparative Biology
The Transmission of Digenetic Trematodes: Style, Elegance, Complexity1
1 Wake Forest University, Winston-Salem, North Carolina 27109
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Traditionally, the field of parasitology has dealt with eukaryotic animals, to the exclusion of viruses, bacteria, fungi, etc., which is the way it will be approached here. The focus of the present paper will be on certain ecological aspects of the life cycles and life-history strategies employed by the Digenea, a diverse group of platyhelminths that includes some 25,000 species. More specifically, the review will consider the nature of host/parasite interactions within molluscan intermediate hosts and the manner in which these interactions, or lack thereof, function in structuring trematode infracommunities within these molluscan intermediate hosts. Literature in this area suggests that predation/competition may be a significant structuring force for infracommunities in certain marine prosobranchs, but not others, and that temporal/spatial factors may be involved as structuring mechanisms in at least some freshwater pulmonates.
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INTRODUCTION |
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There are approximately 25,000 species of digenetic trematodes, or flukes, the adults of which are obligate parasites in a variety of vertebrate animals, ranging from fishes, to birds and mammals. All trematodes, regardless of their definitive hosts, are flat, they possess a protonephridial osmoregulatory system, an incomplete gut, and are covered by a syncitial tegument through which at least some nutrient resources are absorbed. Despite these, and a number of other morphological and physiological similarities, there is a huge diversity in their size, shape, and behavior, as well as the site of infection within their hosts. Three, representative, monoecious flukes and their sites of infection would include Alaria alaria, from the lung of canines, Crepidostomum cooperi from the pyloric ceca of rock bass, and Echinostoma revolutum from the cloaca of Canada geese. In contrast to these monoecious parasites are several species of Schistosoma, dioecious flukes that live in the mesenteric venous systems of humans and other mammals. In addition to certain basic morphological features of all species of trematodes, one of the most important unifying characters for this group of parasites is their catholic use of molluscs as first intermediate hosts.
The Life-Cycle Pattern
Most authorities agree that the basic life-cycle pattern for digenetic trematodes includes three hosts (Poulin, 1998
; Bush et al., 2001). There is first a definitive host in which the parasite reaches sexual maturity, next a molluscan first intermediate host in which asexual reproduction occurs, and then a second intermediate host, which acts as a vehicle for transfer to the definitive host. Given the central importance of molluscs to the overall biology of digenetic trematodes, this is the point at which the discussion will begin.
Following acquisition of the parasite by the mollusc, a larval stage migrates to a species-specific location, e.g., the hepatopancreas, or gonad, or mantle, depending on the parasite and the host. Once it reaches the final site, the larva transforms into a sporocyst, which is little more than an amorphous, germinal sac. Within the sporocyst, a special form of asexual reproduction, known as polyembryony, then occurs. The product of this clonal type of reproduction will vary according to the species of trematode. The stage produced may be a daughter sporocyst, in which case additional polyembryony will occur; or, it may be a redia. Morphologically, rediae are quite distinctive from sporocysts in possessing a mouth, pharynx, and primitive gut. The presence of these structures means that they can ingest host tissue directly, by tearing and swallowing. They are discriminate feeders, in that they will not consume rediae of their own kind. Rediae are also, however, indiscriminate feeders in the sense that they will ingest host tissue, as well as larval stages of other trematodes that may be present. It is this feeding/predation behavior by rediae that has led some investigators (Kuris, 1990) to suggest that this larval stage may be actively involved in structuring trematode communities inside molluscs. This idea will be given full consideration subsequently.
Intramolluscan development continues with polyembryony in the redia. The final intramolluscan stages produced are known as cercariae. As can be seen in Figure 1, their morphology is exceedingly variable. Each is named by some consistent feature of the tail, or the body, or sometimes both. For example, an echinostome is named for the spines that surround the oral sucker. An ophthalmopleurolophocercous cercaria is named for its eyespots and the finfold on the tail. Not figured is an ophthalmopleurolophofurcocercous cercaria, which is described by the presence of eyespots at the anterior end of the body and a finfold on a forked tail.
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Cercariae emerge through a birth pore on the redia's surface and escape from the snail. The number released can measure into the millions over a period of several months, or even years. With a few species, however, cercariae production may be limited to one every few days. Most cercariae are quite small, but they can range up to several mm in length.
Host seeking by cercariae is not a random process, and is stimulated by light, gravity, turbulence, and rarely by chemicals released by the second intermediate host (Combes et al., 1994). The second intermediate host may be an invertebrate, e.g., an aquatic insect or a crustacean, usually benthic, or it may be a vertebrate, most typically a fish or an amphibian. Some species do not require a second intermediate host, but may penetrate the definitive host directly (schistosomes), or may encyst in the open on vegetation (fasciolids), or may encyst in the very host in which they are produced (some echinostomes). Generally, however, cercariae are short-lived and always non-feeding.
Once the cercaria enters the second intermediate host, it sheds its tail and becomes a metacercaria, which is little more than a miniature, but sexually immature, adult, that may, or may not, encyst. Some growth may occur in the second intermediate host, but not always. An interesting feature regarding the relationship between metacercariae and their second intermediate hosts is how benign it may be on the one hand and how virulent it may be on the other. For example, metacercariae of Posthodiplostomum minimum, occur in the internal organs of bluegill sunfishes. It is not unusual to see several hundred of these metacercariae in the heart, liver, and spleen of these hosts, yet there is no apparent effect on the body condition or on long-term survivorship of the bluegills. In contrast, metacercariae of Uvulifer ambloplitis in the flesh/muscle of bluegill sunfishes produce a disease known as "black spot," that not only reduces the body condition in these hosts, but any fingerling with more than 50 metacercariae will not survive the following winter (Lemly and Esch, 1984). All three of the bluegills in Figure 2 are fingerlings, less than one year of age. The effects of black spot on the middle fish can be clearly seen.
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The next step in the typical, three-host life cycle invariably requires a predatory act by the definitive host. Interestingly, the metacercariae of many species may alter the behavior, or eliminate the protective coloration, of the second intermediate host, in such a way as to make it vulnerable to predation by the definitive host (Bush et al., 2001
). Once consumed by the appropriate definitive host, the metacercaria then migrates to a site, which is specific for that particular species of fluke, and matures sexually.
Both self- and cross-fertilization are known to occur among digenetic trematodes (Bush et al., 2001). Monoecious adults with a three-host life cycle produce eggs that are shed in the feces. A snail intermediate host will ingest eggs of some trematodes. With most of the other species, eggs that gain access to water will hatch, releasing free-swimming miracidia, which are propelled in the water column by cilia. This is a short-lived, and non-feeding, stage that must encounter an appropriate molluscan intermediate host within 24 to 36 hr, or it will die. Generally, host seeking by miracidia includes a complicated behavioral process that is initiated through a combination of light and gravity stimuli. These stimuli place miracidia in the vicinity of appropriate molluscan hosts. Chemicals, usually in the form of short-chain fatty acids, or specific amino acids, which are released from the molluscan host, then attract the free-swimming miracidia. Parasite recruitment by the mollusc is not, therefore, accidental.
As alluded to earlier, there is considerable variation in the size, shape, and behavior of digenetic trematodes. The classic case of behavioral modification involving flukes is associated with Dicrocoelium dendriticum, which is found in the bile ducts of sheep throughout the world. Eggs of D. dendriticum shed from infected sheep are ingested by terrestrial snails in which the usual progression of intramolluscan development then occurs. The parasite apparently irritates the snail, causing it to produce and release small, sticky balls of slime from its salivary glands. Inside these slime balls are cercariae of the fluke, nicely encased in a ‘mini’ aquatic habitat, albeit a temporary one. The slime balls are apparently delicacies to ants, which readily ingest them, and thereby acquire the parasite. Almost all of the parasites migrate into the hemocoel where they become metacercariae. However, one or two of the cercariae also invariably migrate to the sub-esophageal ganglia of the ant where they alter the behavior of their hosts. As the ant grazes toward dusk, air temperatures begin to drop. For an infected ant, when the declining air temperature hits a certain threshold, its jaws become locked in a closed position. If the jaw closes shut on a blade of grass, it will remain there, locked throughout the dusk, night, and into the next morning, until the air temperatures rise and the ant's jaws can again be opened. While the ant is attached to the blade of grass, it is vulnerable to being accidentally ingested by a grazing sheep. An interesting aside to this story is evidence suggesting that the metacercariae in the sub-esophageal ganglia are not capable of developing into adults even though their siblings in the hemocoel will. Although this is not biological altruism, it is very close to it.
As indicated at the outset, all trematode life-cycle patterns, other than those involving three hosts, are thought to be derived. Several of the economically-, medically-important species have two-host cycles, with cercariae that directly penetrate the surfaces of their definitive hosts. These would, for example, include the three to five species of Schistosoma that infect the blood-vascular systems of humans where they produce the highly debilitating, and sometimes fatal, disease known as schistosomiasis.
Several trematodes have four-host life cycles. One of these is the hemiurid fluke Halipegus occidualis. For the last 17 yr (for a review, see Esch et al., 1997), various aspects of this parasite's biology/ecology have been studied in a small, North Carolina impoundment, known as Charlie's Pond. This parasite is one of the most remarkable trematodes of which we are aware, for several reasons, including among others its complex, four-host life cycle. Adults of H. occidualis exhibit striking site fidelity, always occurring under the tongues of their definitive hosts, the green frog Rana clamitans. So strong is this site specificity that they may actually attach, one on top of another. One of the advantages for this particular site of infection is that adults of H. occidualis can be enumerated easily, and without killing the host to do it. This is the only adult trematode of which we are aware that can be counted in this manner. It also means that the adult parasite's population size can be easily manipulated. Moreover, it can be followed in time simply by toe-clipping the frog and subsequently recapturing it, then counting the parasites again. Because adults can be so easily counted, we have undertaken a number of population studies (Wetzel and Esch, 1997; Esch et al., 2001). The results of these investigations clearly show that sizes of fluke populations can increase and decrease quite rapidly, even overnight. We have evidence indicating that the instant increases in population densities are the result of recruiting heavily infected dragonflies, the parasites' third intermediate host. Dramatic decreases are believed to occur when tissues under the tongues of green frogs become inflamed and are sloughed. When this happens, the adult parasites attached to them are also sloughed, representing a unique form of density-dependent regulation of the parasite population.
The first intermediate hosts of H. occidualis are pulmonate snails, Helisoma anceps, in which non-swimming, cystophorous cercariae (in these cercariae, the body of the parasite is within a highly-modified tail) are produced. The process of infecting an ostracod second intermediate host is an absolutely remarkable phenomenon (Zelmer and Esch, 1998). When an ostracod's mouthparts puncture the surface of the cystophorous cercaria, there are osmotic pressure changes inside the cyst wall. These osmotic changes cause the explosive release of a so-called delivery tube, which instantaneously penetrates the gut of the ostracod. Almost simultaneously, the body of the parasite is shot through the tube like a cannonball into the ostracod's hemocoel. Another important feature in the life cycle of H. occidualis is that the cystophorous cercariae do not swim. However, these cercariae also remain infective to the ostracod for several days, unlike free-swimming cercariae, which die within a matter of a few hours. The ability to remain infective for a longer period of time than most other cercariae rests with the anhydrobiotic condition in which the body of the cercaria remains until it gains access to the ostracod's hemocoel. Development of the parasite then proceeds with the acquisition of water. Halipegus occidualis can develop to a fully infective metacercaria in the ostracod under laboratory conditions but, under natural conditions, it does not use the ostracod to reach the frog host. We doubt in fact that green frogs can actually see an ostracod, let alone intentionally prey on one.
However, when a dragonfly nymph ingests an ostracod with the developing metacercariae, development to the point of becoming infective will occur enterically in the dragonfly. Then, when a green frog consumes the dragonfly, the cycle is completed. The dragonfly is, therefore, a paratenic host, one that is used by a parasite to bridge an ecological, or trophic, gap.
Just as bizarre as the four-host life cycle of Halipegus occidualis, is the one-host cycle of Plagioporus sinitsini, an opecoelid trematode (Dobrovolny, 1939). The Plagioporous story actually began in 1939 when Dobrovolny studied this parasite in a southeastern Michigan stream. He found that P. sinitsini in Michigan had a 2-host life cycle. In his system, the cystophorous cercariae, instead of being shed, remained within the daughter sporocyst where they encysted, becoming sequestered metacercariae. These daughter sporocysts, containing encysted metacercariae, were then voided in the feces of the snail. The life cycle proceeded when the voided sporocysts were consumed by benthic-feeding fish definitive hosts. Recently, P. sinitsini was found in several, small mountain streams in North Carolina (Barger and Esch, 2000). In these systems, adults of P. sinitsini occur in the gall bladders of rosyside dace, Clinostomus funduloides. Typically, eggs will be voided in the feces of the dace, hatch, and release free-swimming miracidia. The miracidia will then penetrate prosobranch snails, Elimia symmetrica, where they will transform first into mother sporocysts, which will give rise to daughter sporocysts via polyembryony. Daughter sporocysts produce stubby-tailed, inch worm-like, cotylocercous cercariae. Like Dobrovolny (1939) in Michigan, we also found in North Carolina that these cercariae can remain sequestered inside the daughter sporocyst and encyst, becoming metacercariae. However, in our mountain stream system, we found that metacercariae could also continue development to the adult stage while still inside the daughter sporocyst. Not only do P. sinitsini become adults in E. symmetrica, but eggs are produced and hatch inside the daughter sporocysts, releasing free-swimming miracidia. Daughter sporocysts with already hatched miracidia are then released to the outside in the snail's feces.
In effect, cercariae of P. sinitsini have three transmission venues available (Fig. 3). First, a cercaria of P. sinitsini can follow what must be the normal pathway from snail, to larval insect, to fish definitive host. Second, it can encyst inside a daughter sporocyst as a metacercariae, be voided with the sporocyst, and then be consumed by the benthic-feeding definitive host, rosyside dace. Or, third, and the most intriguing of the three alternatives, a cercaria may proceed with development all the way to the adult stage while still sequestered within the sporocyst, produce eggs that can hatch and release miracidia, then be voided with the snails' feces. By following this pathway, miracidia are immediately ready to infect other snails, thus by-passing two hosts in the parasite's life cycle, and creating the opportunity for direct, snail-to-snail transmission. We would also note that this is not progenesis or neotony since the development of P. sinitsini is not short-circuited in any manner. All of the normal developmental stages are still present here; it is just that only one host is now required for completion of the cycle. Moreover, we know this is a functional life cycle in that P. sinitsini has been found in parts of the stream where rosyside dace are not known to occur.
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PARASITE COMMUNITIES: THE NESTED HIERARCHY |
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We want to now move on to another facet of host-parasite interactions, one that involves the way in which trematode populations and communities are, in fact, organized. Most ecologists who study free-living organisms accept the idea that a population can be defined as a group of organisms, of the same species, occupying a given space, in time. However, the application of this definition to parasitic organisms has several special problems. For example, do all life-cycle stages of a single parasite species within a given ecosystem represent a population, or, do all individuals of a single parasite species within a single host constitute a population? Most populations of free-living organisms increase in size through reproduction, or immigration, or both. In contrast, most adult helminths within a given host can increase in numbers only through immigration (=recruitment). Moreover, in a population of free-living organisms, there is usually at least the potential for the free flow of genetic information during the organisms' sexual cycles. However, among helminth parasites, e.g., trematodes, cestodes, nematodes, and acanthocephalans, this is not the case. Thus, genetic information can flow only among sexually active, adult helminths within an individual definitive host. True, there is a potential for gene flow between all parasites within an ecosystem, at some point in time, but the fact that adult helminths are sequestered in a given host during their time of sexual reproduction nonetheless radically reduces the opportunity for genetic exchange. All of these problems in defining the nature and scope of parasite populations can be extended to parasite communities in the same way.
These issues have been conceptually resolved (Esch et al., 1975; Margolis et al., 1981; Bush et al., 1997) through the development of what has been termed a nested hierarchy (Esch and Fernandez, 1991). Let us handle the population problem first. Each rectangle in Figure 4 represents a frog definitive host. And each star in a rectangle is an individual parasite of the same species. The stars in a single rectangle represent an infrapopulation. At the next level of organization is the component population. All of the parasite infrapopulations within a single host population in an ecosystem would comprise the component population, e.g., all of the H. occidualis infrapopulations in green frogs within Charlie's Pond are the component population. At the most inclusive level is the suprapopulation (Fig. 5), represented by all of the life-cycle stages of H. occidualis in the pond. Here, we would include all of the adults, the intramolluscan stages of the parasite, the metacercariae, etc. It is not difficult to understand why it is so important to approach the population dynamics of any parasite species within the framework of the nested hierarchy. The structuring forces, be they biotic or abiotic, are, for the most part, totally different at each hierarchical level, and, since they can be easily separated, their study can be facilitated.
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The organization of parasite communities parallels that of parasite populations. Thus, all of the parasites of all species within a single host, e.g., the stars, triangles, or circles within a single rectangle, are referred to as an infracommunity (Fig. 6). Three different infracommunities are represented here. A parasite component community would include all of the species' infrapopulations within a single host species in an ecosystem, e.g., all of the different parasite infrapopulations within all of the green frogs in Charlie's Pond. For example, a single green frog might be host to three species of parasites, and another might have two. The component community in these three rectangles, or frogs, would thus include three species of parasites, but in different combinations within each frog. Finally, a compound community (Fig. 7) would encompass all of the individuals in all of the life-cycle stages of all species within a given ecosystem, and represent, by far, the most complex parasite community entity within our pond.
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All of this may appear like unnecessary jargon, but over the years, it has become widely accepted as a useful way of understanding and interpreting both the population and community biology of parasitic organisms. When a person studies competitive interactions among parasites, for example, it is clearly understood that this is referring to an activity that is operating at the infrapopulation, or infracommunity, levels. The outcome of such interaction may have implications at the infrapopulation, or infracommunity, levels in terms of egg output, stunting, exclusion, or spatial distribution, and also at the component community level in terms of species richness or diversity. The point is, this hierarchical approach provides not only a method for instantaneous recognition of pattern, it is also important because processes, both spatial and temporal, involved in organizing at each hierarchical level, can be easily separated and examined. And this is what we want to do now, briefly consider the infracommunity dynamics of trematodes in their molluscan hosts.
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STRUCTURING FORCES AT THE INFRACOMMUNITY LEVEL |
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One of the earliest investigations to examine the structure of trematode infracommunities in molluscs, was that of Cort et al. (1937)
, in Douglas Lake and Burt Lake in the northern part of lower Michigan. The question they asked in that study can be simply stated. In modern terminology, it would be, how complex are trematode infracommunities in their snail hosts? They also asked, what is the maximum number of species of larval trematodes that a single snail can possess at the same time? Based on their work, and on the hundreds of others that have been done since 1937, we now have an answer for both questions. First, trematode infracommunities are not very complex, in fact, they are rather depauperate. Second, the maximum size of a trematode infracommunity is four species. According to a recent review by Esch et al. (2001), quadruple infections in a single snail have been seen just three times in the hundreds of thousands of snails that have been examined by investigators all over the world since Cort et al. (1937).
Arising from these very simple questions is another. This one, however, is much more complex and has been much less definitively answered than those asked by Cort et al. (1937). To understand the nature of this question, we should explain that within a given ecosystem, of let's say average complexity, the trematode component community can be rather large. In other words, the diversity of a trematode component community can be fairly large in, for example, a population of Cerithidea californica along the California coast (Kuris, 1990) or Illyanasa obsoleta in a Delaware mudflat (Curtis and Hubbard, 1993), or Helisoma anceps in a North Carolina farm pond (Crews and Esch, 1986; Fernandez and Esch, 1991). In these systems, the number of species of digenetic trematodes ranges from eight to 20, all of them cycling through one of these snail species. Yet, in each of these systems, the maximum number of trematodes infecting a single snail has been four (Esch et al., 2001). The new question thus becomes, what explanation can we provide for these depauperate trematode infracommunities?
A number of possible explanations have been offered for the occurrence of depauperate infracommunities. Careful examination of these explanations will show that they fall into two categories, one based on competitive/predatory interactions among the larval trematodes, and another that includes just about everything else. The major advocates of the competition/predation school include Armand Kuris and Kevin Lafferty, U.C.-Santa Barbara, and, to a lesser extent, Wayne Sousa, U.C.-Berkeley. All three of these investigators have worked extensively with the marine prosobranch, C. californica. The foundation for their assertion relies on the presence of predatory rediae in the life cycles of certain digenetic trematodes, although they couch the argument supporting their position within the framework of competition. As was described earlier, rediae possess a mouth, a muscular pharynx, and a primitive gut. They consume host tissue by tearing and ingesting it directly. This consumption is indiscriminate in that they will not only ingest host tissue, they will also consume larval stages of other trematodes, which they may encounter. Kuris (1990) and Lafferty (1993) have generated evidence that species of trematodes with larger rediae are dominant over those with smaller rediae, or just sporocysts, and have constructed elaborate dominance hierarchies grounded on these observations. In their model of competitive exclusion based on predatory interactions, one of their fundamental assumptions was that a large number of miracidia invade snails more or less simultaneously, initially producing many snails with multiple infections. Competition/predation, they contend, would then proceed and exclusion would result. A serious difficulty with this assumption is that they have no data regarding rates of parasite recruitment for C. californica. In contrast, studies by Curtis (1996) and Curtis and Tanner (1999) on I. obsoleta strongly indicate that parasite recruitment by this snail, at least, is quite slow, too slow for exclusion to produce the outcome predicted in the Kuris model.
We concur that the dominion of rediae in organizing trematode infracommunities is real, but we strongly assert that depauperate trematode infracommunities observed in most studies have a multitude of explanations. For example, Sousa (1990) investigated the component trematode community in C. californica at two sites in Bolinas Lagoon in northern California between 1981 and 1988. Whereas he generated evidence that species with rediae tended not to co-occur, he also concluded that spatial and temporal heterogeneity were important factors in producing depauperate infracommunities.
Perhaps the strongest arguments for spatial and temporal heterogeneity as structuring forces among trematode infracommunities in marine prosobranchs comes from a long series of studies by Curtis and his colleagues on I. obsoleta along the coast of Delaware. As noted earlier, Curtis (1996) and Curtis and Tanner (1999) have aggressively asserted that trematode colonization rates by molluscan hosts are very slow, even in habitats where trematode prevalences were high and multiple infections were frequent. They pointed out that if competition between species was common, then it should occur under these conditions. However, they determined that, even if species composition changes occurred at the rate of 10% per year, it would mean that, on average, an infracommunity might see a new species interaction only once in every 10 yr. Curtis (1996), for example, released 1,400 individually marked and uninfected I. obsoleta at Cape Henlopen, Delaware. He found the recruitment of trematodes into the marked snails to be only 1.6% per year, far too slow to conclude that competition could be a structuring force at the infracommunity or component community levels in this snail species.
In Charlie's Pond, North Carolina, the trematode infracommunities in the freshwater pulmonates, Helisoma anceps and Physa gyrina, were exhaustively studied from 1983 through 1996 (for review, see Esch et al., 1997). One of the interesting findings in these studies was the strong similarity in the trematode infracommunities in these two pulmonates with respect to number of species and the occurrence of congeners (Fernandez and Esch, 1991; Snyder and Esch, 1993). As can be seen in Table 1, there are nine species of flukes in H. anceps and six species in P. gyrina. The similarity in the component communities of the two snail species is clear. However, the dynamics of the trematode infracommunities in the two host species were in striking contrast to each other. For example, Fernandez and Esch (1991) examined close to 5,000 H. anceps, using a clever mark/release/recapture technique devised by Goater et al. (1989). They found just seven double infections among 1,485 infected snails. With a variety of laboratory and field procedures, they concluded that a combination of temporal and spatial factors were responsible for establishing the depauperate infracommunities in H. anceps, not competition/predation. Another unique aspect of their study was the observation that the life span of H. anceps was approximately 12 mo. This meant that the entire component community in H. anceps had to be re-established each year, since the entire cohort of snails was lost within a period of about six weeks each summer. Indeed, between 1983 and 1996, seven of the nine species were consistent members of the component community in H. anceps. In contrast, P. gyrina lives for about three months in Charlie's Pond and are being recruited and turned-over constantly (Snyder and Esch, 1993). These investigators examined 1,181 P. gyrina using the same procedures employed by Fernandez and Esch (1991). Approximately 40% of the P. gyrina were infected with at least one of six species in its component community. In contrast with H. anceps, however, nearly 20% of the infected P. gyrina had double and triple infections, including a high proportion of one species with a redia in its life cycle. Using a simple laboratory protocol, Snyder and Esch (1993) were able to establish, without any question or doubt, that there was no evidence for dominance in these multiple infections.
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Despite our bias regarding structuring mechanisms for trematode infracommunities in molluscan hosts, we are certain the discussions will continue unabated. Earlier in this presentation, we framed the debate as competition versus everything else. Whereas we realize we are not being completely fair with this representation (Fig. 8), the flow of parasites among these various hosts represents the full context of everything else. Based on the complexity of parasite flow in an ecosystem, a larger question is whether the competitive processes that occur within single hosts are strong enough to extend away from snails and influence the entire component community? Or, in contrast, does pressure exerted from the periphery press in on the structure of trematode infracommunities within individual snails? If competition in snails is the dominant force, then we need to know who are the ‘top dogs,’ and how they have achieved this dominance. If competition is insignificant, then all of the complexity of parasite flow within an ecosystem requires attention. Whereas reality probably lies somewhere in between these extremes, we are confident that it tends more toward the latter scenario. Finally, the complexity illustrated here is magnified by our strong contention that each arrow in the diagram is evolutionarily independent of all the others. This is another way of stating that the development of infracommunity patterns in each species of snail has evolved independently. These processes are solely related to the unique biology of the snail host, in combination with the life-history characteristics of each trematode species in the component community of a given ecosystem. Collectively, we believe these interactions serve to illustrate the style, elegance, and complexity of transmission as involved with digenetic trematodes.
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FOOTNOTES |
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1 From the Symposium Living Together: The Dynamics of Symbiotic Interactions presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 3–7 January 2001, at Chicago, Illinois.
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Barger, M. A., and G. W. Esch. 2000. Plagioporus sinitsini (Digenea: Opecoelidae): A one-host life cycle. J. Parasitol, 86:150-153.[Medline]
Bush, A. O., J. W. Fernandez, G. W. Esch, and J. R. Seed. 2001. Perspectives in parasitology: The ecology and diversity of parasites. Cambridge University Press, Cambridge.
Bush, A. O., K. D. Lafferty, J. M. Lotz, and A. W. Shostak. 1997. Parasitology meets ecology on its own terms: Margolis et al. revisited. J. Parasitol, 84:575-583.
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